Download pdf - Michigan State University

ANNUAL
REVIEWS
Further
Quick links to online content
Ann. Rev. Entornol. 1984. 29:471-504
Copyright © 1984 by Annual Reviews Inc. All rights reserved
AN EVOLUTIONARY AND
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
APPLIED PERSPECTIVE OF
INSECT BIOTYPES
S. R. Diehl} and G. L. Bush
Departments of Entomology and Zoology, Michigan State University, East Lansing,
Michigan 48824
Benjamin Walsh (174) was probably the first to seriously consider the status of
insects that morphologically resemble one another so closely that they can only
be distinguished on the basis of subtle biological traits such as preference for or
the ability to survive on different hosts. Most of Walsh's "phytophagic
varieties" now fall under the rubric "biotype," a term employed primarily by
applied biologists to distinguish populations of insects and other organisms
whose differences are due to a very wide range of underlying causes. The
significance of biotypes for both evolutionary and applied fields is not general­
ly appreciated. Our objective is to integrate the current concepts used by
evolutionary biologists to describe various patterns and levels of differentiation
in insects with the views of the applied biologist. A classification system of
insect biotypes, based on the mechanisms underlying their differentiation, is
outlined below. We also consider the significance of biotypes in adaptation,
speciation, and pest management.
A MATTER OF TERMINOLOGY
Biotypes are most commonly entomophagous or phytophagous parasites or
parasitoids distinguished by survival and development on a particular host or by
host preference for feeding, oviposition, or both. Other insect biotypes differ in
diurnal or seasonal activity patterns, size, shape, color, insecticide resistance,
migration and dispersal tendencies, pheromone differences, or disease vector
IPresent address: Department of Entomology, University of Massachusetts, Amherst, MA
01003.
471
OOtltl-4170/R41O1 01 -0471 $07.00
472
DIEHL & BUSH
capacities
(49, BOa). All of these diverse biological differences have been
used to designate populations as biotypes in the literature. Asexuality has also
been a pivotal trait used for differentiating biotypes
(47), but limitations of
space prohibit a discussion of this category here. Although we recognize the
usefulness of the biotype concept, we believe more accurate terminology will
improve communication and understanding. Because the term biotype has been
so loosely applied in the literature, its descriptive power has been greatly
diluted. We therefore urge that more precise terminology be employed to
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
reflect the mechanisms underlying biotype differentiation. In our system, a
biotype may be classified into one or more of the following five categories: (a)
nongenetic polyphenisms, (b) polymorphic or polygenic variation within
populations, (c) geographic races, (d) host races, and (e) species.
Polyphenisms, also called phenocopies or ecomorphs, occur when the same
genotype produces different phenotypes under different environmental condi­
tions
(94, 1 38). In contrast, genetic polymorphisms consist of discontinuous
phenotypes among individuals within a freely interbreeding population that are
the result of allelic variation of a frequency higher than can be maintained by
recurrent mutation
(94). Allelic differences at a single locus may appear
continuous and overlapping due to environmental variation. Polygenic varia­
tion is now recognized as having the same underlying genetic basis as polymor­
phic variation except that many loci, each contributing a small phenotypic
effect, underlie continuous differences.
The status of geographically isolated biotypes, called geographic races
(semispecies or subspecies), is difficult to establish because the differences
observed may or may not be sufficient to ensure reproductive isolation if the
races become sympatric. The related term "ecotype" (ecological race) is
occasionally used when populations within a plant or animal species in the
same habitat in different localities are similar in morphology, ecology, or
behavior
(144, 147), presumably because of convergent selection.
Host races are a more controversial subject and their definition warrants
careful consideration, as they play a pivotal role in the evolution and speciation
of parasitic organisms. We define a host race as a population of a species that is
partially reproductively isolated from other conspecific populations as a direct
consequence of adaptation to a specific host. The basis of isolation may involve
genetically based differences in host preference (when mating occurs on the
host) or many other factors such as allochronic barriers that arise as a direct
result of phenological differences among hosts [modified from (16, 20,
44,
75)]. Nongenetic (polyphenic) differences such as induced host preference or
seasonal mating times may also contribute to reproductive isolation, although,
by themselves, they are unlikely to bring about substantial isolation. Although
we favor the provisional designation of populations specializing on different
hosts in allopatry as "geographic host races," their true evolutionary status will
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
473
remain questionable (as is true of all forms of geographic races) until reliable
tests indicate whether they will fuse or coexist in sympatry. Adaptation to
different hosts may conceivably lead to the development of sexual isolation by
a divergence in courtship behavior, but the conditions necessary for this
process are very restrictive and host race formation by this mechanism is
probably unlikely (20) . Host races may not necessarily exhibit variation in
other traits such as morphology or allozyme frequency.
In contrast, Mayr (95) has defined host races (biological races) as "non­
interbreeding sympatric populations that differ in biological characteristics but
not, or scarcely, in morphology." As Mayr questions the existence and mode of
origin of host races, he qualifies his definition by stating that they are "sup­
posedly prevented from interbreeding by a preference for different food plants
or other hosts." However, because host races by this definition no longer
interbreed at all, they have already reached the stage where they should be
recognized as distinct biological species by Mayr' s own criteria (94). We prefer
to retain a closer correspondence to the common usage of the term "race" as it is
employed by human population geneticists who consider a race to be "a
subdivision of a species formed by a group of individuals sharing common
biological characteristics that distinguish them from other groups" (25). In
addition, a comparison to human races, which frequently do not freely inter­
breed in sympatry owing to culturally transmitted preferences, emphasizes that
racial differences may sometimes be sustained by nongenetic mechanisms.
Jaenike (76) has attempted to extend and refine Mayr's definition of host
races. He views host races as "populations of a single species" with "greatly
reduced gene flow," a criterion slightly less extreme than Mayr's more restric­
tive requirement that the populations be "noninterbreeding." laenike distin­
guishes between host races and sympatric host-associated sibling species by
stating, "if gene flow were restricted solely or primarily because of differential
host preference, then these would constitute host races." We argue that this
definition is inappropriate, however, as we see no valid reason for specifically
excluding host preference differences from the large suite of characters that can
be involved in maintaining reproductive isolation between host-specific sibling
species. Polyphagous species, host races, and host-associated sibling species
should only be distinguished based on the degree of reproductive isolation and
restriction of gene flow, irrespective of whether the isolating mechanism is host
preference, host-associated allochronic isolation, or some other form of
assortative mating that arises as a direct result of the use of different hosts.
Recognizing that these categories continuously blend into one another, it
may be difficult to rigidly categorize examples in nature. Because there is at
least a potential for occasional gene flow between races, selection must be
responsible for the development and maintenance of host race differences in
ecology and behavior (20) Host races seldom, if ever, depend on host prefer. .
474
DIEHL & BUSH
ence alone as a basis for their differentiation. A constellation of divergent
selective forces simultaneously act on each host race. These include temporal
differences in host availability that may influence the timing of diapause,
chemical differences among hosts that affect survival ability. as well as host­
associated variation in rates of parasitism, predation, competition, disease, and
interactions with microorganisms. Some of Jaenike's criteria for demonstrating
the existence of host races are impractical and arbitrary, and further discussion
of suggested alternatives is presented elsewhere (44). It would be rare indeed if
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
only a single trait was responsible for host race formation ( 17, 20, 44).
It is implicitly assumed in discussions of biotypes in the literature that these
consist of conspecific populations differing in some biological trait. However,
it is often the case that more intensive study demonstrates that the populations
actually represent different species.
Species are generally regarded as natural populations that are reproductively
isolated from one another [Walsh in ( 1 4);(94)] and that follow distinct and
independent evolutionary paths (142). Species that morphologically resemble
each other so closely that they can be recognized only after careful study of
biochemical, cytological, or behavioral traits are called sibling species. The
existence of sufficient genetic isolation between biotypes to warrant species
designation can be established with certainty only in situations where the
different populations occur sympatrically without substantial interbreeding or
introgression. While failure to interbreed under laboratory conditions with
proper controls (Le. reproduction is normal within each population) usually
does indicate that populations are isolated in the field, the converse is not
necessarily true. Many animal species freely interbreed in captivity, although
they never do so under natural conditions ( 1 4, 1 77).
The five described categories that account for most of the biological entities
now covered by the broad term "biotype" are not mutually exclusive. Many
biotypes are at various stages of evolutionary divergence and thus provide some
of the best opportunities for unraveling the complicated processes underlying
speciation. It is unfortunate that biotypes have been ignored for so long by
evolutionary biologists; the latter have focused more on animals such as
Drosophila, whose biology is unrepresentative of the many parasitic and
parasitoid insects and mites that gain their resources from other species and
cause some damage, however small, to their host ( 1 20) .
A LOOK AT SOME EXAMPLES
Environmentally Induced Variation (Polyphenism) in Biotypes
A wide variety of biotypes have been identified in applied and evolutionary
research in which the observed variation has a nongenetic, environmentally
induced basis. Environmental induction affects a wide range of traits including
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
475
morphology, behavior, and patterns of diapause. A dramatic example is the
solitary and gregarious "phases" of several locust species whose extremely
detrimental outbreaks have plagued agriculture since their earliest descriptions
in The Old Testament. The phases differ in color, morphology, and behavior.
These differences are continuous, inducible, and partially reversible in the
lifetime of a single individual, primarily by crowding but also by temperature
and humidity (86, 1 68). Unusually large amounts of rainfall enhance plant
growth, and an improved nutrient supply leads to the persistence of large, dense
populations for several generations, which induces the phase change. Howev­
er, the full phenotypic range is not inducible within the lifetime of a single
individual but can be selected for over several generations, thus illustrating
how various biotype categories sometimes overlap. Evidence indicates this trait
is inherited by a maternal cytoplasmic mechanism.
"Seasonal polyphenism," wherein a species goes through a regular yearly
cycle of changes in morphology or host plant use, is known in several insect
orders (138). For example, the control of the production of alate versus
apterous forms in aphids is influenced by temperature, photoperiod, and
feeding on different species of plants or different parts of the same plant ( 1 04).
Seasonal variation in ovipositor length, associated with host use, has been
reported in hyperparasitic gall wasps of the genus Torymus (3). This polyphen­
ic variation is beneficial because the longer ovipositor of spring generation
Torymus enables them to hyperparasitize the correspondingly larger galls of
their spring hosts. Similar host induction occurs in the entomophagous para­
sitoid Trichogramma semblidis, in which individuals reared on certain hosts
exhibit marked differences in wing and antennal structure (131). Other dramat­
ic examples of diet-induced polyphenism occur among the social insects,
whose castes are genetically identical and differentiate because of nutrition
(179). Several scale insect biotypes, formerly placed in different genera, have
been shown to result from polyphenic change by cross-rearing on different host
species or plant parts ( 100).
There is evidence that polyphenism can involve the interaction of three or
more trophic levels. Certain species of parasitic Hymenoptera are capable of
developing on a herbivorous host only when the herbivore is feeding on a subset
of its natural host plant range (121) . Since insect parasitoids often locate their
herbivorous hosts by first orienting to cues emanating from the host plant or
habitat ( 1 7 1 ), the herbivore's susceptibility to this source of mortality can be
host-induced (44). It has long been thought that co-occurrence of potential
hosts in the same habitat may be more important than host systematic affinity in
determining parasitoid attack (37).
SYMBIOTIC MICROORGANISMS AND THE INDUCTION OF BIOTYPES
Multitrophic-Ievel interactions with symbiotic microorganisms may be another
476
DIEHL & BUSH
way that host-associated biotypes can develop without a genetic change in the
insect. Although differences in adaptive traits among closely related or conspe­
cific insects have not yet been shown to be due to the presence of different
symbionts, considerable evidence indicates this potential (80) . In some cases,
however, these differences may not be exclusively induced, as genetic change
in the insect may be required to accommodate microorganisms. Virus particles
injected into the host during oviposition by entomophagous parasitoid wasps
suppress the host's cellular immune response and prevent encapsulation (5 1 ) .
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
Similarly, resistance to bark beetle attack i n pines involves the production of
chemicals that are toxic to the beetles' symbiotic fungus ( 1 24), and microor­
ganisms have been implicated in the synthesis of bark beetle pheromones
(22).
Microorganisms generate volatile attractants that are used by the insect to
locate suitable hosts
(52) and that have been implicated in the nutrition of
(135)], and
cactiphilic Drosophila ( 150), the onion maggot [(92) but see
Rhagoletis flies ( 1 29). Four trophic levels are involved in the case of a
gall-forming insect that uses a symbiotic fungus to physically inhibit attack by
an entomophagous parasitoid ( 175) . In other instances, parasitoids may be
detrimentally infected with entomophagous microsporidia acquired from their
host (6 1 ) . Changes in symbiotic microorganisms can also lead to speciation via
"cytoplasmic" isolation involving male infertility in one or both directions in
reciprocal crosses. Cytoplasmic isolation has recently been reported to occur
among both sympatric and allopatric populations ( 1 1 8).
THE INDUCTION OF SEMIOCHEMICALS
Differences in chemicals which
mediate interactions among organisms have been shown to be environmentally
induced by host plants in a number of organisms. Pheromone production is
affected in the boll weevil (65), bark beetles [(7 1 ) but see ( 1 80)], and Creatono­
tos moths ( 1 34). Chemicals in a herbivore's diet may be concentrated and
released unaltered and subsequently used as kairomones by parasitoids (72).
The behavior associated with pheromone deposition can also vary on different
hosts. For example, a Hylemya fly deposits oviposition-deterring pheromone
only on a host plant where competition for larval food is intense (183). Without
knowledge of the facultative nature of this behavior, genetic differences or
even sibling species might have been suspected.
LEARNING AND THE MODIFICATION OF INSECT BEHAVIOR
Since differ­
ences in host preference and other behaviors are often the major attributes used
to distinguish insect biotypes, it is necessary to consider the possible modifica­
tion of behavior by experience ( 1 , 1 13) . Several distinct kinds of "learning"
have been described including larval induction of host preference (79) and food
aversion learning (42). Preimaginal conditioning, or the "Hopkins Host Selec­
tion Principle," occurs when environmental stimuli during larval stages influ-
477
INSECT BIOTYPES
ence the behavior of the holometabolous adult insect. Most putative examples
of this form of conditioning can be explained by alternative mechanisms. In a
few cases, larval experience is the most likely cause of variation in adult
behavior, although the magnitude of these changes is usually rather small.
For example, it has been suggested that what appears to be preimaginal con­
ditioning might really occur as an adult insect emerges from its puparium or
cocoon in the vicinity of its host. That olfactory preference in Drosophila is
at least partly due to larval experience was shown by washing all traces of
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
the conditioning media from larvae prior to pupation
(165). Another criti­
cism, that selection underlies the change in behavior, is unlikely when prefer­
ence does not appreciably change after the first generation of conditioning
(146).
Learning in vertebrates is disrupted by chemicals that interfere with RNA or
protein synthesis, and preimaginal conditioning of oviposition preference in
Drosophila for peppermint oil or benzaldehyde is similarly blocked by acti­
nomycin c (which inhibits RNA synthesis) in the larval medium
(172). Recep­
tor sensitivity in adult blow flies is affected by sugars present during larval
development (43); this illustrates one possible mechanism that might explain
how experience at the larval stage influences adult behavior. Another mis­
understood aspect of both larval induction and preimaginal conditioning con­
cerns the range of hosts to which the insect is conditionable. For example,
Manduca and Heliothis larvae show altered preferences for hosts previously
eaten only when induced with plants within the natural host range
(79).
Originally, preimaginal conditioning was strictly limited to natural hosts, but
later studies employed unnatural hosts or artificial stimuli. It is well established
that the behavior of adult insects can be adaptively modified by environmental
stimuli experienced during the adult stage
INDUCED DIAPAUSE AND PHENOLOGY
(1, 113, 123).
While it is known that temperature,
photoperiod, and genetic factors influence diapause
(159), a few studies show
that the use of different hosts by phytophagous insects may nongenetically
(44,
144, 181). For example, when Papilio zelicaon is reared in split-brood experi­
induce some of the phenological differences observed among organisms
ments at identical temperatures and photoperiods on one of its host plants, the
propensity to enter diapause is lowered (143); this is adaptive because this host
is available for oviposition later in the season.
Polyphenisms thus play an important role in the development of insect
biotypes. Induced phenotypes represent one of the ways insects can adaptively
respond to variation in the environment. Polyphenism affecting phenology and
host choice may reduce gene flow between populations inhabiting different
hosts or habitats and thus reinforce genetically based isolating mechanisms
during the early stages of host race formation and speciation.
478
DIEHL & BUSH
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
Genetic Polymorphism and Polygenic Variation in Biotypes
The best understood case of genetic polymorphism in biotypes concerns the
interactions between virulence genes in the cecidomyiid Hessian fly, Mayetiola
destructor, and resistance genes in one of its major host plants, domesticated
wheat. The fly, introduced from Europe, reaches epidemic proportions on
some wheat cuItivars. Biotypes of the Hessian fly differ in their capacity to
stunt and survive on different cultivars of wheat ( 1 12).
At present, ten Hessian fly biotypes have been isolated either in laboratory
selection experiments or from natural populations (57, 149). It has been
suggested that virulence in this insect is controlled by recessive, nonallelic
genes, whereas the thirteen known resistance genes in wheat are mostly
dominant or partially dominant (68; J. H. Hatchett, personal communication).
Since there are thirteen genes presently identified in the plant for resistance,
there are potentially 213 or 8,192 possible fly biotypes (genotypes) if each
biotype differed in at least one gene specifically match �ng one of the host's
thirteen resistance genes. Because of this exponential relationship between the
number of resistance genes and possible biotypes, it is apparent that, as the
former increases, the potential number of biotypes rapidly becomes effectively
infinite and the utility or feasibility of biotype designations becomes question­
able. Thus far, only a small fraction of this potential diversity has been directly
assayed. In most of the experiments designed to identify biotypes, only four
resistant wheat varieties have been utilized, each of which contains a different
resistance gene or a pair of genes (57). Using these four resistant varieties to
assess the fly's genotype, there are a total of24 or 1 6 possible combinations of
susceptibility or resistance that can be exhibited and therefore 1 6 possible
biotypes. However, just because individuals respond similarly to these
varieties, they need not be identical in their response to other resistance genes.
In fact, biotypes used in most studies are composed of strains that have been
"purified" by several generations of rearing on wheat varieties with different
resistance genes and a hybridization test in the F4 generation to eliminate
heterozygous individuals. Therefore, the apparent simplicity and distinctive­
ness of the biotypes may be at least partly due to the relatively simple genetic
criteria used to categorize individuals in laboratory assays.
Hybridization of Hessian fly biotypes has been claimed to indicate evidence
of a "gene-for-gene" interaction between the fly and its wheat host (58, 67)
similar to the genetic interactions that have been extensively studied in plant­
parasitic fungi and other disease organisms (38). This means that "virulence"
loci in the fly match "resistance" loci in the plant in a one-to-one relationship.
However, this hypothesis has only been directly tested in two biotype hybrid­
ization experiments (58, 67), and the possibility of co-recessive alleles at a
single locus is equally consistent with the results. At most, these experiments
positively demonstrate the existence of only two or three independent virulence
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
479
loci in the fly. If all known biotypes were genetically analyzed for gene
independence, this apparently simple system might reveal more complicated
genetic interactions, such as allelic inheritance, pleiotropy, epistasis, or incom­
plete dominance, that do not conform to the simple gene-for-gene model.
Additional insight is needed into the underlying cause of resistance and
susceptibility. For example, recent data indicate that in some cases a large
fraction of the larvae on unstunted plants survive (149). Therefore, this resis­
tance may sometimes be more appropriately classified as a "tolerance" mecha­
nism. The genetic interactions of a gall-forming insect such as the Hessian fly
may involve very different biochemical interactions compared to insects that
feed by chewing and macerating their hosts. "Non-preference" may also be an
important factor contributing to susceptible and resistant wheat varieties, but
the only two studies on this subject give conflicting results (112). The potential
importance of nonpreference is probably most significant when considering
wild grass hosts of the Hessian fly. We are not aware of any studies of the role
of these hosts conducted since the 1950s, but there have been several reports in
the Midwest of Hessian flies that have established populations on wild grasses
and subsequently moved onto domestic wheat (R. L. Gallun, personal com­
munication). The wild grasses may be especially important as "refuges" for the
normally trivoltine fly during the parts of the season when wheat is too mature
for infestation (153). Early studies of wild host plants indicated that Hessian
flies reared from wheat will oviposit and successfully develop on a large
number of wild grasses as well as on domestic barley and rye (107, 112). The
possibility of sympatric host races has not been directly addressed in the
Hessian fly. Therefore, host preference of the Hessian fly should be reex­
amined using modem behavioral choice assays conducted under conditions at
least somewhat resembling those in the field.
Wheat arose from diploid domesticated or wild ancestors as a result of two
interspecific hybridizations events. Since these hybridization events involved a
limited number of individuals from each wild parent species, the amount of
genetic variation in domesticated wheat may be greatly reduced. Because
wheat is a hexaploid, the chance of resistance genes occurring at different
(nonallelic) loci may be enhanced, since the plant begins with a minimum of at
least three duplicated genes after hybridization. Historically, only a small
number of wheat genotypes had been planted over large areas (i.e. monocul­
ture) (7). This practice has promoted the development of genetically distinct
Hessian fly biotypes that cause severe damage to the crop. In recent years the
use of resistant wheat varieties has kept damage by the Hessian fly to low
levels, but future pest evolution overcoming this defense remains a perennial
possibility and therefore presents an important monitoring responsibility.
Another intensively studied example of genetic variability for both plant
resistance and insect virulence is the rice brown planthopper system (48).
480
DIEHL & BUSH
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
Nilaparvata iugens is a notorious pest of rice, a cereal crop domesticated
thousands of years ago. This insect feeds only on cultivated rice and closely
related wild forms. Until recently it has been only a minor pest in its year-round
habitat in the tropics. Severe infestation by this insect as well as the viruses it
transmits occurred in the early 1970s in the experimental farms of the Interna­
tional Rice Research Institute in the Philippines. Attack was limited to the
high-yielding varieties and subsequently also occurred in Indonesia and on the
Indian subcontinent. Modem agricultural practices that have made it possible to
grow rice continuously favor the buildup of large planthopper populations.
Moreover, sublethal doses of some insecticides induce a "resurgence" of
planthopper populations by increasing feeding activity, development rates,
adult longevity, and oviposition periods (70).
Varieties of rice differ greatly in their susceptibility to planthoppers, and
presently four "major" resistance genes have been identified ( 1 48). These occur
as two closely linked pairs, with each pair containing one dominant and one
recessive resistance gene. But resistance-breaking biotypes of planthopper
have rapidly developed, first in laboratory selection experiments and soon after
in field populations (148). When planthoppers are classified by virulence in
response to the four known resistance genes in rice, there are 16 possible
biotypes; at present, six of these have been isolated. Some studies have
reported that laboratory colonies of planthopper biotypes differ in morphology
(133, 148) and esterase isozymes (148), but other studies indicate much
overlap in morphology, cytology, biochemistry, and acoustic behavior (27,
91). Distributions of these traits and their genetic heritability in sympatric and
allopatric natural populations in semi-natural habitats and in monocultures is
required to fully evaluate the management and evolutionary significance of this
variation.
Hybridization of planthopper biotypes indicates that resistance-breaking
traits are inherited by a complex polygenic mechanism (40, 148). The biotypes
broadly overlap in virulence, and it is possible to select for the virulence of any
biotype within ten generations starting with individuals of another biotype (40).
Clearly, biotypes of rice brown planthopper are very different from Hessian fly
biotypes where data indicate that discrete differences in virulence are due to
polymorphisms at several major genes. Some authors have suggested that the
biotype concept may be "positiv�ly misleading" for cases involving polygenic
inheritance, as in the brown planthopper. These authors would restrict biotype
designations to simple gene-for-gene relationships (27, 28 , 9 1) . Historically,
the term "biotype" has been so broadly applied, however, that a more restricted
definition at this time seems impractical. Strains of planthopper thus qualify as
biotypes by our general definition, but it is important for both evolutionary and
applied biologists to recognize that this variation is continuous, overlapping,
and has a polygenic basis. The mechanism of resistance in rice also differs from
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
481
that in wheat where "antibiosis" may predominate. Feeding on resistant rice
varieties is greatly reduced due to "nonpreference," and individuals attempt to
migrate to more acceptable plants (148). The distinction between nonprefer­
ence and antibiosis may be largely due to mobility differences, however, as
both nymphs and adults in the brown planthopper can migrate from unsatisfac­
tory hosts, whereas Hessian fly larvae do not have this option and simply die.
Within a small geographic area in Sri Lanka, where large-scale monoculture
is still relatively uncommon, planthopper populations have locally adapted to
domestic varieties or wild rice, as they develop fastest on the variety from
which they are collected (29). This occurs despite potentially large amounts of
gene flow. Although mating among biotypes is random under laboratory
conditions, behavioral preferences for particular rice varieties may act as a
partial intrinsic barrier to interbreeding in the field in sympatry and parapatry.
Such assortative mating facilitates the buildup and maintenance of variety­
adapted races. What appears to be a distinct sibling species of planthopper
occurs in Australia. It is differentiated from other populations in its ability to
infest certain rice varieties and is reproductively isolated by premating
courtship mechanisms (28).
Biotypes of the raspberry aphid, Amphorophora idaei, are also frequently
cited as an example of a gene-for-gene interaction between an insect and its host
plant (13). Populations infesting blackberry are now recognized as a distinct
sibling species (A. rubi) because of consistent differences in chromosome
number (9). Although a gene-for-gene interaction has been claimed, selection
of resistance genes having discrete and major effects may largely be a result of
practical considerations in raspberry breeding (82). The only hybridization
study among aphid biotypes (13) produced inconsistent results and was ham­
pered by very small sample sizes. The claim that a gene-for-gene interaction
occurs between alfalfa clones and biotypes of the spotted alfalfa aphid has not
been tested by genetic analyses, as the aphid biotypes are exclusively parthe­
nogenetic (106). Another example of biotypes involving genetic variation
within a population is the chestnut gall wasp, Dryocosmus kuriphilus. Intro­
duced into Japan from China, it initially caused severe damage but was
controlled by use of resistant chestnut varieties. The lifetime of this resistance
was relatively short, however, and new resistance-breaking biotypes soon
developed (140).
A directly analogous situation involves the black pineleaf scale, Nuculaspis
cali/ornica, which may have genetically adapted to variation among individual
ponderosa pines (50). Populations of these sessile scales appear to be adapted to
overcome the unique spectrum of defenses exhibited by their particular host
tree. This conclusion was initially based on experiments measuring the survi­
vorship of groups of scales transferred from infested to uninfested trees at a
different site. Individual trees differ in susceptibility to scale attack, and demes
482
DIEHL & BUSH
of scales collected from individual trees differ in their average ability to
colonize new uninfested host trees. More importantly, a significant interaction
was observed: some scale demes that were generally poor colonizers when
tested on most trees did exceptionally well on trees that exhibited high resis­
tance to most other scale demes. Striking differences among individual trees in
their susceptibility to attack have also been reported in the pine tortoise scale
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
( 1 10).
Further research on black pineleaf scales has focused on the em:cts of gene
flow and different densities of scales on the pronounced female-biased sex ratio
in these insects. An elaborate model has been proposed to explain the increase
in male frequency that occurs over time as the population adapts to an indi­
vidual tree (2, 2a). This model assumes that differential mortality between the
sexes in these haplo-diploid organisms is due to the fact that the diploid females
are more genetically variable than the haploid males, that this variability
confers a higher average fitness by some mechanism of heterosis, and that a
reduction in genetic variability in both sexes over time is due to selection by the
host tree's chemistry. These assumptions have not been tested, however, and
the genetic basis for adaptation to individual trees is unknown. It has been
proposed that the increase in male frequency confers an additional adaptive
advantage by reducing gene flow from immigrant males that are unlikely to be
adapted to the tree. However, an alternative explanation for the increase in
male frequency could be due to the fact that males, unlike females, mature into
winged adults capable of directed, long-distance dispersal and active foraging
for mates at new host trees. As an infestation progresses, mean fecund­
ity decreases, and thus it may become advantageous to produce greater num­
bers of male offspring, which are better dispersers. This alternatiye scenario
is consistent with a report that red pine scale crawlers (immature stages) are
more likely to disperse by becoming airborne at high infestation densities
(96). The black pineleaf scale system has often been cited as a definite case
of genetic variation for host utilization within an insect species, despite the
fact that Alstad & Edmunds (2a) acknowledge "that alternative hypotheses
remain."
Insight into the molecular basis of virulence has been provided by genetic
studies of insecticide resistance, which is most often due to single major genes
that influence several detoxification enzymes simultaneously in the house fly,
Musca domestica ( 1 17). Resistance is associated with a chromosomal inversion
adjacent to but not containing the resistance gene that appears to act as a
regulator of several detoxification enzyme genes located in the inversion. By
altering the position of the enzyme genes on the chromosome, the inversion
changes the pattern of expression (i.e. a "position effect"). Another example
where a chromosomal rearrangement may influence a character important to an
organism's fitness occurs in Anopheles stephensi, where daily emergence times
are strongly correlated with an inversion (34).
INSECT BIOTYPES
483
Resistant and susceptible strains of house fly also differ in their sensitivity to
insecticides as inducers for specific detoxifying enzymes not otherwise present
(or detectable) in the insect's tissues. Evidence from receptor-binding studies
indicates that induction is due to an alteration of a receptor protein, but it is not
known whether this is due to a single base pair substitution (point mutation) or
whether a larger deletion, addition, or rearrangement of the receptor protein
gene is involved. Present evidence therefore supports the hypothesis that
insecticide resistance by metabolic detoxification in the house fly involves a
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
change in gene regulation that arises both from a position effect due to a
chromosomal inversion and from a structural change in a receptor protein that
regulates the induction of detoxification enzymes. These results are relevant to
the study of insect-plant chemical interactions, as these receptor proteins in
Heliothis virescens (117) and Periplaneta americana (109) also react with toxic
plant allelochemicals.
Many studies of polymorphism by evolutionary biologists have focused on
patterns and functions of chromosomal rearrangements in adaptation and spe­
ciation
(19, 173, 176). The maintenance of polymorphism has been one of the
central issues in the field of "ecological genetics," which has been concerned
with the evolution of mimicry and adaptive coloration such as the famous
examples of "industrial melanism" in Biston betularia and other moths (99).
Genetic mechanisms of diapause (159) and patterns of migration and dispersal
(66) have also been investigated in detail. Evolutionary biologists continue to
devote considerable attention to studies of biochemical genetic polymorphism.
These studies have expanded from the initial focus on allozymes and now
include immunological comparisons of proteins and analyses of the genetic
material itself by DNA hybridization, restriction enzyme mapping, or gene
sequencing techniques (21,
46). Although gene sequencing is presently too
complicated and costly for screening the large numbers of individuals needed
for population genetic studies of insect biotypes, continued advances will make
these methods more accessible in the near future. Their greatly enhanced
genetic resolution should eventually lead to a significant improvement in our
understanding of the evolutionary process that should correspondingly facili­
tate the management of insect pests.
Geographic Variation and Biotypes
Geographic variation among races and sibling species of entomophagous
parasitoids is especially important because of implications for biological con­
trol. Differences in host utilization occur in two biotypes of the ichneumonid
parasite Bathyplectes curculionis, both of which were introduced from
Utah
and now are allopatric in northern and southern California (132). These
biotypes differ in their susceptibility to encapsulation by each other's host
weevil. Virus-like paritcles that have been observed in the ovaries of this
species
(154) may suppress the host's immune response (51). Without further
484
DIEHL & BUSH
study it cannot be determined whether this geographic variation is due to a
genetic change in the insect, its symbiotic virus, or both. Although these
biotypes are presently allopatric in California, they may have originated sym­
patrically in Utah, or they may even be presently reproductively isolated in
sympatry and thus constitute distinct species.
In most cases, the evolutionary status of geographically isolated populations
differing in host utilization or other traits cannot be determined with certainty.
If the populations were united under natural conditions in sympatry, they might
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
either lose their distinction through interbreeding or maintain it due to some
form of assortative mating and then be considered distinct species. Such a test
has been performed with Comperiella bifasciata (39). Two geographic "races"
of this parasitic wasp have been imported into California for biological control
of scale insects. A Chinese race prefers red scale but can develop in yellow
scale, whereas the Japanese race strongly prefers yellow scale and virtually
never completes development in red scale. The two races are morphological­
ly indistinguishable and although hybridizing readily in the laboratory they
"maintain their distinctness" in California, where they occur in sympatry,
because of differences in host preference or utilization ability (39). Too little is
known about the past and present distribution of C. bifasciata in China, Japan,
and other areas to determine whether the two forms presently occur in sympatry
or if the differences between the races originally developed in sympatry or after
geographic isolation.
A number of forest pest insects have also received considerable attention
with respect to geographic variation in host utilization and other traits. The
spruce budworm complex (Choristoneura spp.) includes representatives wide­
ly distributed across North America. Some of the described species are sympat­
ric, whereas others are separated geographically, and different classifications
have been proposed based on mophology, host plants, and more recently
allozyme comparisons
(152). Genetic differences are generally very small,
sometimes within the range usually associated with conspecific populations
rather than with separate species, and the morphological, host plant, and
allozyme bases of classification do not always agree. Similar allozyme com­
parisons of Dendroctonus bark beetles indicate that intraspecific geographic
variation may be extremely limited over a large part of the western United
States
(151). In contrast, the use of different host plants within a IO(;al popula­
tion can lead to significant changes in gene frequency, as is discussed further in
the context of host races.
Sympatric or parapatric ("microgeographic") differences occur in East Afri­
can Aedes aegypti mosquitoes. A light-colored domestic form breeds inside
village huts in pots while a dark form breeds outside in tree holes
(56). The
forms differ in allozyme frequency, which indicates that gene flow between
them is restricted because of habitat preference, despite their close proximity.
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
485
Similar local variation between indoor and outdoor populations of Anopheles
mosquitoes has been detected for inversion frequencies (35). These results are
consistent with several evolutionary studies of local variation in Drosophila.
Differences in alcohol tolerance between strains from inside versus adjacent to
a wine cellar occur in spite of evidence of gene flow between them (97). In
another study, both inversion and allozyme frequencies varied significantly
over very short distances and were attributable to habitat preferences rather
than extremely strong selection pressure ( 162). These results show that dif­
ferentiation at even weakly selected or nearly neutral loci can occur in the face
of considerably more gene flow than suggested by Mayr (94) and others who
have argued that barriers "must be virtually impermeable" (56) . An equally
in-depth understanding of dispersal, selection, and popUlation structure is
needed for populations of phytophagous and entomophagous parasites.
The evolution of green lacewings of the genus Chrysopa involves geographic
variation coupled with a divergence in habitat utilization (160) . C. carnea and
C. downesi are predaceous as larvae and feed on honeydew as adults. They are
sympatric over a large area in the northeastern US, but C. carnea prefers a
deciduous open-field habitat, whereas C. downesi is found in conifers. They
also differ in coloration and seasonal activity periods in ways that would adapt
them to their respective habitats. It has therefore been suggested that these
species originated by a mechanism that we would label sympatric "habitat race
formation." However, the discovery of rather strong behavioral barriers involv­
ing differences in acoustic communication during courtship (73), combined
with recent studies of geographically isolated populations from the western US
that are closely related or conspecific with C. carnea or C. downesi ( 1 60), must
also be taken into consideration. In a similar case of habitat race formation, a
group of spittlebugs exhibits a color polymorphism that is very tightly associ­
ated with habitat and host plant differences in adjacent "minimeadows," often
less than 12 m apart (64). The polymorphism has remained constant for nine
years as a result of strong stabilizing selection, very sedentary behavior, or very
consistent habitat or host selection, which would restrict mating between
parapatric populations.
Biotypes have been described based on geographic variation in the European
com borer, Ostrinia nubilalis, which was introduced to North America from
Europe during the early part of this century. It soon became apparent that
populations across North America differed in voltinism, diapause, and degree
of polyphagy (24, 1 4 1 ) . Three "ecotypes" (biotypes) are generally recognized
as occurring in northern, central, and southern states. Populations in the cooler
northern climates exhibit only one generation per year while populations in
southern states have two or more. Morphometric variability is correlated with
biotype groupings, but rearing geographically isolated strains under identical
conditions has shown that much of this variability is environmentally induced
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
486
DIEHL & BUSH
polyphenism (26). In contrast, differences among biotypes in voltinism persist
in identical environments and are known to have a strong genetic basis involv­
ing sex-linked nondominant inheritance (141). In com, resistance to O. nubila­
lis has been attributed to one, two, or more genes differing among inbred lines
(111). Breeding for resistance is complicated in areas sustaining multivoltine
attack, because first and later generations feed on different parts of the plant and
none of the presently identified sources of resistance are effective against both
generations.
Little attempt has been made to integrate information about the European
com borer that is derived from evolutionary studies of pheromone differences
with information from studies on ecotypes. Ostrinia nubilalis in Europe and
North America consists of two distinct pheromone strains that differ in the ratio
of isomers produced by calling females (24). Com borer populations from New
York and Italy utilize a 3 :97 ratio of Z and E isomers, whereas populations from
most other localities in Europe and North America exhibit a 97:3 ratio,
indicating multiple introductions of this insect from different parts of Europe.
Furthermore, reproductive isolation may exist between pheromone strains that
occur sympatrically in Pennsylvania; there are small but statistically significant
differences in allozyme frequencies, and laboratory hybridization tests indicate
strong premating isolation but an absence of postmating isolation (24). The
feasibility of managing the com borer by release of biotypes with diapause
genes that are maladaptive in the climate of the release area has been questioned
(141). A more promising integrated control program might be devised by
combining information on pheromone strains into the management strategy.
For example, care needs to be taken that insects released will respond to the
pheromone composition of local com borer populations.
Another important aspect of the com borer's biology that has received little
attention in recent reviews is the use of alternative host plants. Early studies
indicated that some (but not all) com borer popUlations were very polyphagous
in North America (24, 163). It should be remembered that com is indigenous
to the new world and was introduced into Europe a few centuries ago. Geogra­
phically isolated populations in France were reported to feed exclusively on
maize or wild Artemesia vulgaris, respectively, for many generations in the
absence of alternative hosts at either site or in the "broad belt" separating them.
Despite the prolonged restriction of each population to different hosts in
allopatry, the populations differed only slightly in oviposition preference
(163). This result and others discussed below suggest that divergence of host
preference in allopatry may be a very slow or even unlikely process, contrary to
the view of Mayr (94) and others that geographic isolation is predominant in the
development of host-associated races and species.
Geographic variation in the ability to survive and grow on different hosts has
recently been reviewed for several other Lepidoptera (136). The data do not
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
487
permit any simple generalizations, since contrasting results have been obtained
for different species groups. Populations of the polyphagous species Callosa­
mia promethea were collected from different parts of its range and tested for
their survival ability on a number of hosts. Survival was generally high,
irrespective of geographic origin or whether the host naturally occurs near the
collection site. In contrast, some tentative evidence of geographic variation in
host utilization exists for a more specialized species, Papilio cresphontes.
An extensive survey of geographic variation has also been reported for the
eastern tiger swallowtail , Papilio glaucus, which ranges across North America
(137). It is represented by two subspecies that overlap narrowly across the
northern US and that differ in color, morphology, diapause, and host plant
utilization abilities. Survival rates and growth performance on different host
plants have been tested for several populations across this species ' range.
Substantial differences were found, but the interactions are complex and very
different geographic patterns are observed for different hosts . For example,
tulip tree is a major host of the southern subspecies (P. g . glaucus) throughout
much of its range, and populations of this subspecies readily feed and develop
on it (even populations from southern Wisconsin where tulip tree does not
occur). In contrast, populations of the northern subspecies (P . g . canadensis)
from northern Wisconsin cannot utilize this host. Quaking aspen is readily used
by P. g . canadensis but not by the southern subspecies (even where this host
naturally occurs at some southern localities). Still other hosts can be used by
both subspecies, and there are differences within the southern subspecies in
ability to feed on spicebush. Sharp distinctions in voltinism and diapause exist
between the subspecies across a very narrow band in mid-Wisconsin , which
precisely coincides with a recognized plant transition zone. However, neither
oviposition preference nor geographic variation in suitability within host plant
species, both of which may be very important for interpreting the evolution of
host utilization in this species, has yet been investigated. It is also questionable
whether these subspecies diverged in parapatry by shifting from a bivoltine to a
univoltine life cycle across the plant transition zone without any absolute
geographic barriers to gene flow or whether this occurred after total isolation in
allopatry. It should be further noted that the possible existence of sympatric
host races has not been investigated in the Papilio glaucus system .
Similar patterns of geographic variation in host utilization have been re­
ported for the Colorado potato beetle . Leptinotarsa decemlineata. which is
native to North America and feeds on about ten wild solanaceous plants and on
the introduced cultivated potato. Overall, this relatively specialized beetle
exhibits little variation in host utilization ability among 12 geographic popula­
tions, but it does differ latitudinally in diapause (74). Beetles from Arizona,
however, are unique in their ability to feed on a local wild Solanum species and
also exhibit the best development of all populations when tested on seven other
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
488
DIEHL & BUSH
hosts. However, since tests have not been reported for beetles collected from
different host plants in sympatry where host distributions overlap , the conclu­
sion that this example indicates that host race formation is far more common
under conditions of geographic isolation than in sympatry (55) is unsupported.
In fact, development of host preference may be less likely in an isolated
population that is only exposed to a single host than among sympatrk host races
that are constantly exposed to two or more potential hosts but may face severe
consequences if a wrong choice is made.
Populations of Colias philodice eriphyie, an oligophagous butterfly, shifted
from natural legume hosts to the legume alfalfa about 90 years ago ( 1 57).
Populations on wild hosts and alfalfa are usually geographically isolated today
and differ in ability to feed and develop as larvae on their respective hosts but
not in oviposition preference. Once again, the absence of a change in oviposi­
tion preference is not surprising, because individuals from wild or alfalfa
populations do not usually encounter each other's host in nature. It would be of
interest to test whether differences in oviposition preference , phenology , or
host-utilization ability exist between individuals using different sympatric wild
host plants. The bimodal distribution observed for an oviposition preference
measure within a population using two wild hosts in Parlin, Colorado ( 1 58) is
consistent with the existence of sympatric host races. But since oviposition
preference tests used only females captured as adults whose larval host cannot
be determined, the data available do not permit this question to be addressed.
Differences in host preference among geographically isolated populations of
Euphydryas editha butterflies have been characterized as "ecotypic variation"
(144) indicating that heritable differences exist among popUlations inhabiting
ecologically different habitats (e.g. alpine meadows versus dry chaparral).
Populations specialize on one host even when other potential hosts are present,
and sometimes this avoidance is due to ant predation. In other cases, the insect
appears to behave suboptimally with respect to oviposition preference and the
suitability of host plants for larval development. This may be due to a lag in
evolutionary response to a successional change in the plants present in the
habitat (144). There does not appear to be a strong ' correlation between
oviposition preference and the larval host of the emerging female (144). It has
been reported that popUlations survive and grow better on their most commonly
used larval host plant compared to the common host of conspecific populations
120 km away ( 1 25). Equally sensitive studies have not been carried out within
sympatric populations to compare the suitability of primary and secondary
hosts. A difference in larval development time and consequently in adult
emergence among popUlations feeding on different hosts may result in partial
nongenetic allochronic isolation (144), which would favor sympatric host race
formation. However, several other aspects of the life history favor a more
flexible, oligophagous diet. For example, host plants are ephemeral both within
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
489
the lifespan of a single individual over the season (larvae frequently must move
onto different hosts in later instars) and also in the course of plant succession
over several years as hosts change in abundance. Local extinction of butterfly
populations appears to be common, and mating does not always occur in close
association with the host.
In summary, we have found only limited evidence of geographic variation in
traits related to host utilization among insect biotypes. This conclusion is
contrary to that of Fox & Morrow (53), who reviewed primarily phenotypic
variation in host utilization, but in agreement with Gould (63) who has re­
viewed evidence which indicates that, in general, there appears to be at least as
much genetic variation in host preference and survival abilities within sympat­
ric populations of a species as among widely separated allopatric populations.
This occurs despite a possible bias from searching for such variation preferen­
tially among geographic isolates. Differences in diapause among spatially
isolated populations appear to be more common, as might be expected con­
sidering the geographic variation in temperature, photoperiod, and season
length occurring across different climatic zones. These findings are consistent
with sympatric models of speciation but do not generally support the view that
geographic isolation is necessary for the development of races or species of
parasitic insects.
Biotypes and Host Race Formation
It is extremely difficult to positively identify host races because every sus­
pected case has to be checked by careful ecological, behavioral, and genetic
studies. Of the host races that have been described, most occur among groups
of specialized monophagous parasites or parasitoids. For the sake of brevity,
only examples where quantitative or qualitative information is available con­
cerning important aspects of the biological interaction between the parasite and
its host are considered. Earlier descriptive studies are reviewed elsewhere (15,
4 1 , 145, 164, 1 74).
The biology of ectoparasites such as lice or fleas may result in a shift to a new
host that involves elements of both geographic and sympatric host race forma­
tion. Many closely related species or races of fleas have shifted from a bird to a
mammalian host or vice versa. It has been reported that "mammal fleas are not
infrequently found as stragglers on birds of prey, especially owls" (130). These
stragglers may be the initial colonists that eventually give rise to a new species.
Another host transfer has occurred in the biting lice (Mallophaga) of the family
Boopiidae which, with one exception, are confined to marsupials. The excep­
tion is Heterodoxus spiniger, which now occurs on domestic dogs throughout
the world (23). The louse probably shifted to dogs via the wild dingo, which
frequently preys on kangaroo. This marsupial is infested by the clo&ely related
but distinct H. longitarsus. The degree of spatial isolation and restriction of
490
DIEHL & BUSH
gene flow between ectoparasites on different hosts has never been determilled.
Since predaceous dingos or owls may commonly utilize a given prey, gene flow
between diverging ectoparasite populations may be substantial (although pri­
marily in one direction). In this case, the divergence would most closely
approximate the conditions of parapatric or sympatric host race fonnation.
Interesting cases of divergence under conditions somewhat analagous to
sympatric host race fonnation occur in the human louse and in carrion-feeding
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
mites. Two morphologically and biologically distinct fonns of Pediculus
humanus occur on humans; one is adapted to the head and the other to the body,
but whether these originated in sympatry or allopatry is unresolved
(90, 94).
The parasitid mite Poecilochirus necrophori uses different species of carrion­
feeding beetles for phoretic transport. Individual mites exhibit strong genetical­
ly controlled preferences for different beetles
(178), which indicates either a
"carrier polymorphism," racial subdivision by specialization on different car­
rier beetles, or carrier-specific sibling species.
A number of host races have been reported in sexually reproducing Heterop­
tera. Several sympatric races of aphids specialize on different host plants and,
although they hybridize and produce nonnal fertile offspring in the laboratory ,
they do not readily interbreed in nature and are isolated by host choice and
survival differences ( l 05,
139). Populations of the univoltine leafhopper
Oncopsisjlavicollis on different species of birch display an oviposition prefer­
ence for the species of birch from which they are collected, even in mixed tree
stands
(30). A polymorphism in sex chromosomes is also associated with one
of the host races. Evidence indicates that other species of Oncopsis may also be
subdivided into host races
(31). Planthoppers of the Muellerianella group
demonstrate the importance of host shifts in the speciation of parasitic insects,
although the evidence is equivocal as to whether these host shifts are most
likely to have occurred in sympatry or allopatry ( lOa,
47). Host races may also
exist in the obscure scale, Melanaspis obscura, infesting various species of
oaks. Differences in the timing of male development, which is synchronized
with host phenology, prevent interbreeding
(100). Mating occurs on the host
plant, a feature common to many Homoptera and other plant-sucking insect
groups.
In the Coleoptera, plant-feeding Chrysomelidae appear to be particularly
rich in host-specific sympatric races or sibling species. Several cases have been
reported where host specificity is the major isolating mechanism between
populations that freely interbreed in the laboratory. In the Chrysomeia interrup­
ta complex, individuals are often nearly morphologically identical but experi­
ence substantial reductions in survival on hosts other than the one from which
they are collected (14). Because individuals intennediate in morphology exist
in natural populations, thus indicating that hybridization occasionally occurs,
these fonns are host races rather than sibling species. Another case of host races
491
INSECT BIOTYPES
or
sibling species occurs in the ladybird genus Henosepilachna in Japan
(81).
Sympatric populations on different host plants hybridize readily in the labora­
tory and produce fully viable and fertile F 1 offspring. Differences in host choice
are responsible for maintaining distinctness in natural populations. Host races
in both of these species complexes most often occur in sympatry on different
hosts, whereas wide-ranging allopatric populations do not usually differ in host
plants. These distribution patterns are inconsistent with allopatric models
(94)
(20) . Similar cases of
sympatric host races and sibling species occur in other chrysomelids (14)
including Fochmaea capreae, which has host races on birch and willow (87).
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
but agree with sympatric models of host race formation
Rapid host race formation has occurred in a milkweed beetle, Tetraopes
tetrophthalmus (122). A population was found feeding on Asclepias verticilla­
ta, which inhabits cooler soil than A . syriaca and had colonized a ridge of
dredged soil along a stream bank. Mating occurs on the host plant, and beetles
that were infesting A . verticillata had a reduced probability of mating with
beetles infesting nearby stands of A . syriaca.
Genetic and morphological differentiation exists among mountain pine bee­
tles (Dendroctonus ponderosae) on lodgepole and ponderosa pine, thus indicat­
ing the possible existence of host races
(155). There is some evidence that
beetles in mixed tree stands preferentially select their larval host for mating and
oviposition as adults
(5). When sympatric collections from both hosts are
combined, a significant deficiency of heterozygotes occurs at several loci,
which is consistent with substructuring by host races
(151, 155). Populations
from the same host in different areas, however, are sometimes less similar in
allozyme frequencies than populations from different sympatric hosts
(151).
It
is possible that some of these differences may be due to selection by the trees'
chemical defenses, especially at loci such as esterases, which are involved in
detoxification pathways.
Examples of host races in the Lepidoptera include Papilio demodocus, which
infests Citrus and members of the Umbelliferae
(32). Two distinct larval
morphs, whose expression appears to be controlled by a single gene with
modifiers, occur sympatrically on different hosts. The forms interbreed in the
laboratory and there are no differences in survival when reared on each other's
host. In nature there is strong selection by bird predation against the umbellifera
pattern on Citrus and vice versa. Another example of host races differing in
larval color morphs has been reported in the oligophagous larch bud moth,
Zeiraphera diniana (6), Specific color morphs are associated with different
hosts, and each host race is closely synchronized with its host plant, thus
ensuring that first instar larvae emerge during bud break of their respective
hosts. These examples illustrate how host race formation may sometimes be
initiated by factors other than host preference or the ability to feed and develop
on a given host
(20). Sympatric host races have been reported in the codling
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
492
DIEHL & BUSH
moth, Laspeyresia pomonella . Biologically distinct populations occur on ap­
ple, pear, apricot, plum, and walnut ( 1 1 ) , but the status of most of these host
races is uncertain. Evidence of allochronic isolation and differences in oviposi­
tion preference ( 1 1 6) and allozyme frequencies ( 1 14) in sympatric populations
indicate the existence of sympatric or parapatric host races in some localities.
Detailed studies on leafmining ermine moths of the genus Yponomeuta have
uncovered the existence of several closely related monophagous sibling species
and host races. One species, Y. padellus, consists of at least three sympatric
host races that infest different species of Rosaceae (98) and a partially sympat­
ric fourth race that attacks Salix ( 169) . Sympatric host races are interfertile in
laboratory crosses and do not differ in the sensitivity of their larval che­
moreceptors to compounds present in their respective host plants ( 1 70) . Indi­
viduals collected from Prunus spinosa exhibit generally higher pupal weight
and survival on several other host plants than individuals collected from these
hosts (59), which is inconsistent with models of host race formation by
diversifying selection (20) . However, sympatric populations collected from
different hosts differ significantly in allele frequencies at several allozyme loci,
and a genetic analysis using Wright's F-statistics also indicates population
substructuring by host races (98) .
Sibling species complexes are commonly encountered in the Hymenoptera,
many of which include host races (36). Host races have been noted in diprionid
sawflies associated with coniferous trees (85) . Populations on the various hosts
differ in phenology; host preference for feeding, mating, and oviposition; and
survival ability on specific hosts . These traits appear to be under simple genetic
control, although a formal genetic analysis was not undertaken. Additional
examples of host races have been reported in other sawflies (8) . Host races
generally occur in monophagous groups, whereas polyphagous sawflies are
usually widely distributed and show elinal variation in morphology but have no
well defined host-related subdivisions .
Host race formation may be a common mechanism of sympatric speciation in
several parasitoid Hymenoptera (4). For example, sympatric populations of
Aphytis mytilaspidis differ in preference for scale hosts (83) . There is some
evidence of hybrid breakdown in crosses between the two races, which sug­
gests that they may be sibling species, but fertility was not tested using natural
hosts. In another case, Anicetus beneficus may have evolved by a sympatric
host shift to an introduced scale in Japan in the 1 940s ( 1 82). Parasitoids
collected from two different scale hosts are morphologically very similar but
differ strongly in host preference.
Fruit-infesting tephritid flies of the oligophagous genus Rhagoletis have
developed several host races, some in recent times on introduced hosts. In
Europe, R . cerasi infests sweet cherry and honeysuckle berries . The two races
differ in emergence times but are completely interfertile in laboratory crosses
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
493
( 1 0). In North America, adults of R . pomonella from sympatric populations
that infest different hosts emerge at different times in synchrony with the
maturation of their host fruit ( 16, 44, 1 26). Although considerable overlap
occurs, this allochronic isolation may partially reduce gene flow. Variation in
ability to survive on diverse hosts is less pronounced than rates of parasitism,
which vary greatly on different hosts (44) . Host preference differences among
populations from different hosts have been observed in a field cage assay using
branches, leaves, and fruit of each host tree (44). Less pronounced differences
have also been observed in a laboratory assay using individual fruit from
different host trees ( l23a). However, acceptability of different hosts in the
single fruit laboratory assay has been demonstrated to be modifiable by pre­
vious adult experience ( 1 23), so it will be important to investigate the genetic
basis of these behavior differences in order to fully evaluate their implications.
Significant variation in allozyme frequencies has also been observed among
some sympatric populations infesting different hosts (S . R. Diehl and G. L.
Bush, in preparation). However, without "diagnostic" loci, a situation prob­
ably common in recently evolved host races or sibling species, it is difficult to
determine whether observed differences are due to reproductive isolation or to
selection by the host plant acting on larvae infesting different fruit within a
freely interbreeding population. Trace element analysis of adult flies has been
applied in an attempt to directly measure gene flow and host preference in the
field by identifying the larval host plant of adult insects captured while ovipos­
iting or mating (45). Flies collected as larvae in naturally infested apples versus
sour cherries and held as adults in the laboratory following eclosion differ
dramatically in their trace element concentrations. However, preliminary tests
of wild-caught adult flies suggest that adult feeding on honeydew and other
substrates in the field may interfere with a clear resolution of the larval host
plant "chemoprint" in natural populations, which would limit the usefulness of
this technique (44). R . cingulata, R . indifferens, and R . jausta are host specific
on different native Prunus species in North America and have established
populations on introduced sweet and sour cherries that show some evidence of
isolation as host races ( 1 7 , 44). R. conversa in Chile infests native Solanum
tomatillo and has established a host race on introduced S. nigrum, which differs
in morphology, phenology, and host preference (but not in genitalia, metaph­
ase chromosomes, or allozymes) (54).
While most Drosophila are generalist feeders, one species group that infests
rotting cacti may have formed specialized host races. Populations of D .
mojavensis collected from different cacti consistently differ in a chromosomal
rearrangement, even in an area where the distributions of both host plants
nearly overlap (69). Populations of the presumably polyphagous agromyzid
leafmining fly Liriomyza brassicae that have been collected from different
hosts are genetically differentiated in host preference or survival and develop-
494
DIEHL & BUSH
ment ability ( 1 6 1 ). However, the magnitude of these differences is quite small
and thus their biological significance may be limited. Host races have also been
described in plant-parasitic nematodes ( 1 67).
An absence of host races has been noted in several insect groups. Studies of
allozyme variation in polyphagous mushroom-feeding Drosophila failed to
uncover substantial subdivision among populations associated with different
host fungi (77,
89). The ephemeral and unpredictable nature of the fungal hosts
precludes development of host specificity. In order to survive, these multivol­
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
tine flies must regularly use several different hosts because no single host
species is available for an entire season. A similar association of rnultivoltine
life cycles with polyphagous feeding on ephemeral fruit versus host specializa­
tion in univoltine species infesting more predictable hosts is evident in a
comparison of tephritid flies
( 1 84).
Allozyme frequencies in populations of ten oligophagous and polyphagous
geometrid moths collected from different host plants were compared; little
statistically significant differentiation indicative of host race formation was
found
( lO2). Some of the sample sizes in these comparisons were small,
however, and therefore subtle differences in gene frequency might not have
been detected. Furthermore, samples from only a single locality were reported,
and thus relative amounts of variation associated with different sympatric hosts
versus geographic factors cannot be compared. Mating in these moths is not
restricted to specific hosts , and larvae often disperse widely . Some of these
species require very young leaves for food during the first larval instar, so
emergence must be precisely timed to coincide with bud break. The chance of
survival would thus be limited unless larvae can feed on several different hosts,
a factor that would discourage the formation of host races. Several species are
multivoltine, which may further inhibit the development of host specific races
if each host is available in suitable nutritional condition for only a portion of the
insect's seasonal activity period. Allozymes have also been compared in the
fall webworm, which polyphagously feeds on many species of trees (78) . Two
color morphs, which exhibit a weak and overlapping association with different
hosts, are so greatly differentiated that they must be distinct species. In
contrast, no differentiation was found between populations of the red morph
collected from different hosts. Although the sample sizes of this latter compari­
son are adequate, replicates from different geographic sites were not analyzed
so that again the relative contribution of host-associated versus allopatric
divergence cannot be assessed.
Biotypes as Species
One frequent outcome of studies undertaken to clarify the status of what are
believed to be biotypes is the discovery that they are really distinct sibling
species. We mention only a few of the many examples that have been identified
( 14, 1 5 , 4 1 , 1 64),
INSECT BIOTYPES
495
The treehopper Enchenopa binotata was considered a polyphagous species
composed of sympatric host races. But studies involving hybridization, mate
choice, host selection, and allozyme analyses have demonstrated that it is
actually a complex of six species , each associated with a different host plant
( 1 8 1 ) . A primary isolating mechanism is host preference, combined with the
fact that mating occurs on the host. Adults usually do not disperse widely, and
phenological differences appear to be induced by the host plant and to result in
allochronic isolation. Furthermore, reduction of egg hatch and nymphal surviv­
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
al occurs when the treehoppers are reared on host plants utilized by other
members of the complex.
Two biotypes of the purslane sawfly, Schizocerella pilicornis, have been
shown to be distinct species (62). One form of this insect mines and the other
form feeds externally on the leaves of Portulaca oleracea. The entire life cycle
takes place on or under the host. The two forms occur sympatrically but differ
markedly in allozyme frequency, and one locus is nearly diagnostic, indicating
that little or no gene flow occurs between them. Slight differences in morpholo­
gy, emergence time, and onset of diapause also support the conclusion that
these biotypes are distinct species . Although broadly sympatric at present, their
origin is uncertain since they may have been introduced from Europe
(33) .
Divergence of these forms may have been promoted by monogamy, sib­
mating, and inbreeding which commonly occur in haplo-diploid Hymenoptera.
Other previously unrecognized species of Hymenoptera occur in Muscidifurax
raptor, Aphytis mytilaspidus, Diprion polytomum, and other sibling species
complexes ( 3 6 , 1 28) .
Another example of closely related species that have been described as
biotypes occurs in Diabrotica iongicornis (88) . Two forms of this beetle feed
on different hosts, and their geographic ranges overlap considerably. Although
the forms differ in coloration, variation is clinal and not always consistent
within a species . However, studies have revealed host-preference, pheromone,
developmental , and fixed allozyme differences. Present distributions indicate
that speciation probably occurred in sympatry or parapatry, initiated by a host
shift. A comparison with other members of the genus Diabrotica again reveals
that multivoltine species tend to be polyphagous, whereas univoltine groups are
more specialized ( 12).
Procecidochares australis flies form galls on two sympatric composite
plants, Macroanthera and Heterotheca (75). Although fertile F\ and backcross
progeny occur in the laboratory, allozyme, host selection, and survival experi­
ments revealed that the two host races are distinct species . Host preference
appears to be controlled by a major locus , and survival was affected by one or
two genes, although the exact numbers were not established. It should be
noted, however, that even in species that dramatically differ in morphological,
chromosomal, or allozyme frequencies, some hybridization and gene flow may
still occur. For example, where Drosophila pseudoobscura and D . persimilis
496
DIEHL & BUSH
are sympatric, they share 70-85% of their maternally inherited mitochrondrial
genomes in conunon ( 1 19). Where allopatric , they differ completely. These
results strongly imply that hybridization occurs , but this has not prevented
considerable divergence in characteristics controlled by their nuclear genomes.
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
EVOLUTIONARY AND MANAGEMENT PERSPECTIVES
This review reveals a tremendous diversity in the ways insects cope with their
environment through the formation of biotypes. Sometimes this adaptation is
due to nongenetic variation. Other biotypes may differ in traits controlled by
single genes or by polygenic mechanisms. The gene-for-gene model of host­
parasite interactions has not been rigorously tested or demonstrated among
insect biotypes, and its relevance to plant pathogen systems in general (includ­
ing fungal and bacterial disease) has also been questioned (7 , 38). An equally
broad diversity of defenses exists among the plants and animals that serve as
hosts for parasitic biotypes. This array includes many different mechanisms of
"nonpreference," "antibiosis ," and "tolerance" ( 108, 1 1 2), some of which are
induced in direct response to attack (48, 93) . These same mechanisms are also
central to evolutionary models of host-parasite interactions . but different termi­
nology (such as host or habitat selection and survival ability) is usually applied
(16, 20, 1 0 1 , 1 3 1 ).
The study of insect biotypes has contributed substantially to our understand­
ing of host race formation and speciation. Host races occur most often in
monophagous groups in sympatry. Sympatric speciation by host race formation
is most likely when there are genetic differences in host preference and survival
ability on different hosts and when mating occurs in close association with the
host (20) . Existing genetic models of sympatric speciation are biologically
unrealistic for parasitic organisms because they fail to incorporate genes
controlling host selection and disregard the fact that mating is often closely
associated with the host (20). Much of this empirical and theoretical evidence
of sympatric speciation has been overlooked or ignored in recent critiques (56,
76, 1 1 5). For these reasons, the conclusion that sympatric speciation by host
race formation requires extremely restrictive conditions ( 103) is unwarranted.
The diversity of insect biotypes emphasizes that each speciation event is unique
and it is unlikely that any single global model will apply in every case ( 1 8 , 176) ,
contrary to claims that single processes predominate in host shifts (55) or
speciation (56, 1 1 5).
Biotypes have obvious implications for pest management and biological
control , as the failure to recognize distinct populations can have costly and
frustrating consequences (20a, 60, 1 28). For example, an improperly identified
cryptic species that is poorly adapted to local conditions can reduce the
effectiveness of a sterile insect release program (84). The biological control of
weeds has been hampered by the inability to recognize important biological
INSECT BIOTYPES
497
differences among morphologically identical insects ( 1 27), and some biotypes
differ in ability to act as vectors for disease transmission ( 1 66) . Advances in
molecular genetics provide powerful new tools for uncovering this cryptic
variation and should have increasing application in the future (2 1 , 84) .
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
CONCLUSIONS
The term biotype has been so loosely applied to such a wide range of biological­
ly distinct entities that it has extremely little descriptive power. We therefore
urge that future application of this term be restricted to use as a temporary and
provisional designation for cases where biological differences have been
observed between organisms but where the genetic basis and evolutionary
status of the differences have yet to be ascertained. Once research has identified
the underlying nature of the observed variation, more appropriate terminology
should be applied as discussed in this review and further use of the ambiguous
and all-encompassing term "biotype" should be discontinued.
ACKNOWLEDGMENTS
We thank our many colleagues who assisted us in gathering relevant literature,
especially 1 . A. Dohanich and W. A. Gregory . We also thank T. 1. Bierbaum,
R . T. Carde, D. 1 . Futuyma, D. 1. Howard, 1. R . Miller, and R . I . Prokopy for
reviewing earlier versions of the manuscript and C. Presnell for word pro­
cessing and other assistance. Portions of this work were supported by NSF
grant DEB 801 1 098.
Literature Cited
1 . Alloway, T. M. 1972. Learning and
memory in insects. Ann. Rev. Entomol.
1 7:43-56
2. Alstad, D. N . , Edmunds , G. F. 1983.
Selection, outbreeding depression, and
the sex ratio of scale insects . Science
220:93-95
2a. Alstad, D. N . , Edmunds, G. F. 1983 .
Adaptation, host specificity, and gene
flow in the black pineleaf scale. In Vari­
able Plants and Herbivores in Natural
and Managed Systems, ed. R . F. Denno,
M. S. McClure. New York: Academic.
In press
3. Askew, R. R . 1965. The biology of the
British species of the genus Torymus Dal­
man (Hymenoptera: Torymidae) associ­
ated with galls of Cynipidae (Hymenop­
tera) on oak, with special reference to
alternation of forms. Trans. Soc. Br. En­
ramol. 16:217-32
4. Askew, R . R. 1968. Considerations on
speciation in Chalcidoidea (Hymen-
optera) . Evolution 22:642-45
5. Baker, B . H . , Amman, G. D . , Trostle,
G . C. 1 97 1 . Does the mountain pine bee­
tle change hosts in mixed lodgepole and
whitebark pine stands? USDA For. Servo
Res. Note INT. No. 151
6. Baltensweiler, W . , Benzy, G . , Bovey,
P . , Delucchi, V. 1977. Dynamics of
larch bud moth popUlations. Ann. Rev.
Entomol. 22:79-- 100
7. Barrett, J. A. 1 98 1 . The evolutionary
consequences ofmonoculture. In Genetic
Consequences ofMan-Made Change, ed.
J. A. Bishop, L. M. Cook, pp. 209-48.
New York: Academic
8. Benson, R. B. 1950. An introduction to
the natural history of British sawflies
(Hymenoptera, Symphyta). Trans. Soc.
Br. Entomol. 10:45-142
9. Blackman, R. L . , Eastop, V. F., Hills,
M. 1977. Morphological and cytological
separation of Amphorophora Buckton
(Homoptera: Aphididae) feeding on
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
498
DIEHL & BUSH
European raspberry and blackberry
(Rubus spp.). Bull. Entomol. Res. 67:
285-96
10. Boller, E. F ., Bush, G. L. 1974. Evi­
dence for genetic variation in populations
of the European cherry fruit fly , Rha­
goletis cerasi (Diptera: Tephritidae)
based on physiological parameters and
hybridization experiments. Entomol.
Exp. Appl. 1 7 :279-93
lOa. Booij , C. 1. H . 1982. Biosystematics of
the Muellerianella complex (Homoptera,
Delphacidae) in Western Europe. PhD
thesis. Agric. Univ. , Wageningen, The
Netherlands
I I . Bovey, P. 1 966. Le carpocapse ou ver
des pommes et des poires. Entomol.
Appl. Agric. 1 :402-6
1 2 . Branson, T. F . , Krysan, J. L. 1 98 1 .
Feeding and oviposition behavior and life
cycle strategies of Diabrotica: an evolu­
tionary view with implications for pest
management. Environ. Entomol. 10:
826-3 1
1 3 . Briggs, J. B . 1965. The distribution,
abundance, and genetic relationships of
four strains of the rubus aphid (Amphor­
ophora rubi (Kalt. » in relation to a rasp­
berry breeding. J. Hortic. Sci. 40: 10917
14. Brown, W. J. 1959. Taxonomic pro­
blems with closely related species. Ann.
Rev. Entomol. 4:77-98
1 5 . Brues, C. T. 1 946. Insect Dietary. Cam­
bridge , Mass: Harvard Univ. Press
16. Bush, G. L. 1969. Sympatric host race
formation and speciation in frugivorous
flies of the genus Rhagoletis (Diptera,
Tephritidae). Evolution 23:237-5 1
1 7 . Bush, G. L. 1975. Sympatric speciation
in phytophagous parasitic insects. In
Evolutionary Strategies of Parasitic In­
sects and Mites, ed. P. W. Price, pp.
1 87-206. New York: Plenum
1 8 . Bush, G. L. 1975. Modes of animal
speciation. Ann. Rev. Ecol. Syst. 6:
339-64
1 9 . Bush, G. L. 1 98 1 . Stasipatric speciation
and rapid evolution in animals. In Evolu­
tion and Speciation. Essays in honor of
M. J. D. White, ed. W . R. Atchley, D . S .
Woodruff. New York: Cambridge Univ.
Press
20. Bush , G . L . , Diehl, S. R . 1982. Host
shifts, genetic models of sympatric spe­
ciation and the origin of parasitic insect
species. Proc. 5th Int. Symp . Insect­
Plant Relationships,
pp.
297-306.
Wageningen: Pudoc
20a. Bush, G. L. Hoy, M. A. 1983. Evolu­
tionary processes in insects. In Ecologic­
al Entomology, ed. C. B . Huffaker, R. L.
Rabb. New York: Wiley-Intersci. In
press
2 1 . Bush, G. L . , Kitto, G. B . 1978. Applica­
tion of genetics to insect systematics and
analysis of species differences. In Belts­
ville Symposia in Agricultural Research.
2. Biosystematics in Agriculture, ed. J.
A. Romberger, p p . 89- 1 1 8 . New York:
Wiley
22. Byers, J. A . , Wood, D. L. 1 98 1 . Anti­
biotic-induced inhibition of pheromone
synthesis in a bark beetle. Science 2 1 3 :
763-64
23. Calaby, J. H. 1 970. Phthiroptera. In The
Insects of Australia . Canberra: Mel­
bourne Univ. Press
24. Carde, R. T. 1983. The role of pher­
omones in reproductive isolation and spe­
ciation of insects . In Evolutionary Genet­
ics of Invertebrate Behavior, ed. M. D.
Huette\. New York: Plenum. In press
25. Cavalli-Sforza, L. L . , Bodmer, W. F.
1 97 1 . The Genetics of Human Popula­
tions. San Franisco: Freeman
26. Chiang, H. C. 1978. Pest management in
corn. Ann. Rev. Entomol. 23: 1 01-23
27. Claridge, M. F . , Den Hollander, J. 1980.
The "biotypes" of the rice brown plant­
hopper, Nilaparvata lugens. Entomol.
Exp. Appl. 27:23-30
28. Clardige, M . F. , Den Hollander, J . 1983.
The biotype concept and its application to
insect pests of agriculture. Crop Prot.
2:85-95
29. Claridge M. F. , Den HOllander, J . ,
Furet, I . 1982. Adaptations of brown
planthopper (Nilaparvata l.ugens) popu­
lations to rice varieties in Sri Lanka. En­
tomol. Exp . Appl. 32:222-26
30. Claridge M. F. , Nixon, G. A. 1 98 1 .
Oncopsis leafuoppers on British trees:
polymorphism in adult O. flavicollis
(L.). Acta Entomol. Fenn . 38: 1 5- 1 9
3 1 . Claridge, M . F. , Reynolds, W. J . , Wil­
son, M. R. 1977. Oviposition behaviour
and food plant discrimination in leafuop­
pers of the genus Oncopsis. Ecol. En­
tomol. 2: 1 9-25
32. Clarke, C. A . , Dickson, C. G. C . , Shep­
pard, P. M. 1963. Larval color pattern in
Papilio demodocus. Evolution 17: 1 3037
33. Clement, S . L. , Norris, R. F. 1 982. Two
insects offer potential biological con­
trol of common puslane. Calif. Agric.
(March-April): 1 6- 1 8
34 . Coluzzi, M . 1 9 7 2 . Inversion polymorph­
ism and adult emergence in Anopheles
stephens;. Science 176:59-60
35. Coluzzi, M . , Sabatini, A ., Petrarca, V . ,
Di Deco, M . A. 1 979. Chromosomal dif
ferentiation and adaptation to human en­
vironments in the Anopheles gambiae
complex. Trans. R . Soc. Trap. Med.
Hyg. 73:483-97
36. Crozier, R. H. 1977. Evolutionary genet,
,
­
INSECT BIOTYPES
37.
38.
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
SO.
51.
52.
ics of the Hymenoptera. Ann. Rev. En­
tamol. 22:263-88
Cushman, R. A. 1926. Location of indi­
vidual hosts versus systematic relation of
host-species as a determining factor in
parasitic attack. Proc. Entomol. Soc.
Wash. 28:5-6
Day, P. R . 1 98 1 . Genetics of pathogenic
fungi. In Genetics as a Tool in Microbiol­
ogy, ed. S. W. Glover, D . A. Hopwood.
New York: Cambridge Univ. Press
DeBach, P. 1 974. Biological Control by
Natural Enemies. New York: Cambridge
Univ. Press
Den Hollander, 1 . , Pathak, P. K. 1 98 1 .
The genetics of the "biotypes" of the rice
brown planthopper, Nilaparvata lugens.
Entomol. expo appl. 29:76-80
Dethier, V. G. 1 954. Evolution of feed­
ing preferences in phytophagous insects.
Evolution 8:33-54
Dethier, Y. G. 1980. food-aversion
learning in two polyphagous caterpillars ,
Diacrisia virginica and Estigmene con­
grua. Physiol. Entomol. 5:32 1-25
Dethier, V. G . , Goldrich, N. 1 97 1 .
Blowflies: alteration of adult taste re­
sponses by chemicals present during de­
velopment. Science 173:242-44
Diehl, S. R. 1 9 83 . Host race formation
and sympatric speciation in Rhagoletis
(Diptera: Tephritidae). PhD thesis.
Univ. Texas, Austin
Diehl, S. R . , Bush, G. L. 1983. The
use of trace element analysis for deter­
mining the larval host plant of adult
Rhagoletis
(Diptera:
Tephritidae).
Proc. Int. Symp . Fruit Flies. Athens,
Greece: CEC Press
Dover, G . , Flavell , R. B . , eds. 1982.
Genome Evolution. London: Academic
Drosopoulos, S. 1977. Biosystematic
Studies on the Muellerianella Complex
(Delphacidae, Homoptera Auchenor­
rhyncha) . Meded. Landbouwhogesch.
Wageningen 77: 1-133
Dyer, M . I . , Detting, 1 . K., Coleman, D.
C., Hilbert, D . W. 1982. The role of
herbivores in grasslands. In Grasses and
Grasslands: Systematics and Ecology,
ed. 1. R. Estes, R . I . Tyr!, 1. N. Brunken,
10:255-95. Oklahoma: Univ. Okla.
Press
Eastop, V. F. 1973 . B iotypes of Aphids.
Bull. Entomol. Soc. N. Z. 2:40-5 1
Edmunds, G. F. , Alstad, D. N. 1978.
Coevolution in insect herbivores and con­
ifers. Science 199:941-45
Edson, K . M . , Vinson, S. B . , Stoltz, D.
B . , Summers , M. D. 1 98 1 . Virus in a
parasitoid wasp: suppression ofthe cellu­
lar immune response in the parasitoid's
host. Science 2 1 1 :582-83
Ellis, P. R . , Taylor, 1. D . , Littlejohn, I.
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
63 .
64.
65.
66.
67.
499
H. 1982. The role of microorganisms col­
onizing radish seedlings in the oviposi­
tion behavior of cabbage root fly, Delia
radicum. See Ref. 20, pp. 1 3 1-37
Fox, L. R . , Morrow, P. A. 198 1 . Spe­
cialization: species property or local phe­
nomenon? Science 2 1 1 :887-93
Frias Lasserre, D. A. 1 98 1 . Evolutionary
biology ofOtitidae and Tephritidae (Dip­
tera Acalyptratae). PhD thesis. Univ.
Chile (In Spanish)
Futuyma, D. 1 . 1983. Selective factors in
the evolution of host choice by phytopha­
gous insects. In Herbivorous Insects:
Host-seeking Behavior and Mechanisms,
ed. S. Ahmad, pp. 227-44 . New York:
Academic
Futuyma, D. 1 . , Mayer, G. C. 1980.
Non-allopatric speciation in animals.
Syst. Zool. 29 : 254-7 1
Gallun, R . L. 1977. Genetic basis ofHes­
sian fly epidemics. Ann. NY Acad . Sci.
287:223-29
Gallun, R. L. 1978. Genetics of biotypes
B and C of the Hessian fly . Ann. En­
tomol. Soc. Am. 7 1 :48 1-86
Gerrits-Heybroek, E. M . , Herrebout, W.
M., Ulenberg , S . A., Wiebes, 1 . T.
1978. Host plant preference of five spe­
cies of small ermine moths (Lepidoptera:
Yponomeutidae). Entomol. Exp . Appl.
24:360-68
Gonzales, D . , Gordh, G . , Thompson, S .
N . , Adler, 1 . 1979. Biotype discrimina­
tion and its importance to biological con­
trol. In Genetics in Relation to Insect
Management, ed. M . A. Hoy, 1. 1 .
McKelvey Ir. New York: Rockefeller
Found.
Gorske , S. F . , Maddox, 1. V. 1978. A
microsporidium, Nosema pilicornis sp.
n . , of the purslane sawfly, Schizocerella
pilicornis. J. Invertebr. Pathol. 32:23543
Gorske, S. F . , Sell, D. K. 1976. Genetic
differences among purslane sawfly
biotypes. J. Hered. 67:271-74
Gould, F. 1983. Genetics of plant­
herbivore systems: Interactions between
applied and basic study . See Ref. 2a. In
press
Halkka, O. 1978. Influence of spatial and
host-plant isolation on polymorphism in
Philaenus spumarius. Symp . R . Entomol.
Soc. London 9:41-55
Hardee, D. D. 1970. Pheromone produc­
tion by male boll weevils as affected by
food and host factors. Contrib. Boyce
Thompson Inst. 24: 3 1 5-2 1
Harrison, R. G. 1980. Dispersal poly­
morphisms in insects. Ann. Rev. Ecol.
Syst. 1 1 :95- 1 1 8
Hatchett, 1. H . , Gallun, R . L. 1970.
Genetics of the ability of the Hessian fly,
500
68.
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
69.
70.
71.
72.
73.
74.
75.
76.
77.
78.
79.
80.
DIEHL & BUSH
Mayetiola destructor, to survive on
wheats having different genes for resis­
tance. Ann . Entomol. Soc. Am. 63:
14@-7
Hatchett , J. H . , Martin, T. J., Livers, R.
W. 1 98 1 . Expression and inheritance of
resistance to Hessian fly in synthetic hex­
aploid wheats derived from Triticum
tauschii (Coss) Schmal . Crop Sci.
2 1 :73 1-34
Heed, W. B. 1 978. Ecology and genetics
of Sonoran Desert Drosophila. In
Ecological Genetics: The Interface, ed.
P. F. Brussard. New York: Springer­
Verlag
Heinrichs, E. A . , Aquino, G. B . , Chel­
liab, S . , Valencia, S. L . , Reissig, W. H .
1982. Resurgence of Nilaparvata lugens
(Stal) populations as influenced by
method and timing of insecticide applica­
tions in lowland rice. Environ. Entomol.
1 1 :78-84
Hendry, L. B . , Piatek, B . , Browne, L .
E. , Wood, D. L . , Byers, J . A . , e t al
1 980. In vivo conversion of a labeled host
plant chemical to pheromones of the bark
beetle Ips paraconfusus. Nature 284:85
Hendry , L. B . , Wichmann, J. K . , Hin­
denlang, D. M . , Weaver, K. M. , Korze­
niowski, S. H. 1 976. Plants-the origin
of kairomones utilized by parasitoids of
phytophagous insects? J. Chem. Ecol.
2:271-83
Henry, C, 1983 . Sexual behavior of
green lacewings. In Biology of Chrysopi­
dae, ed. Y. Semeria, T. R. New. Amster­
dam: Junk. In press
Hsiao, T. H. 1982. Geographic variation
and host plant adaptation of the Colorado
potato beetle. See Ref. 20, pp. 3 1 5-24
Huettel, M. D . , Bush, G. L. 1972. The
genetics of host selection and its bearing
on sympatric speciation in Proceci­
dochares (Diptera: Tephritidae) . En­
tomol. Exp. Appl. 1 5 :465-80
Jaenike, J. 1 98 1 . Criteria for ascertaining
the existence of host races. Am. Nat.
1 1 7:830--34
Jaenike, J . , Selander, R . K. 1979. Eco­
logical generalism in Drosophilafalleni:
genetic evidence. Evolution 33:741-48
Jaenike , J . , Selander, R. K. 1980. Dn the
question of host races in the fall web­
worm, Hyphantria cunea. Entomol . Exp .
Appl. 27:31-37
Jermy T. , Hanson, F. E . , Dethier, V. G .
1968. Induction of specific food prefer­
ence in Lepidopterous larvae . Entomol.
Exp . Appl. 1 1 :2 1 1-30
Jones, C. G. 1 983. Microorganisms as
mediators of plant resource exploitation
by insect herbivores. In A New Ecology:
Novel Approaches to Interactive Sys-
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.
91.
92.
93 .
94.
terns, ed. P. W. Price, C. N. Siobodchi­
koff, W. S. Gaud. New York: Wiley­
Intcrsci.
Katakura, H . , Hinomizu, H . , Yamamo­
to, M. 1 98 1 . Crossing experiments
among three ladybird "species" of Heno­
sepilachna vigintioctomaculata complex
(Coleoptera, Coccinellidae) feeding on
thistles and/or blue cohosh. Kontyu
49:482-90
Keep, E. 1 98 1 . Resistance to aphids in
temperature fruit crops. Proc . 9th In/.
Congr. Plant Prot., Washington 1 : 1 7882
Khasimuddin, S . , DeBach, P. 1976.
Biosystematic and evolutionary statuses
of two sympatric populations of Aphytis
mytilaspidis, Hym . : Aphelinidae Enlo­
mophaga 2 1 : 1 1 3-22
Kitto, G. B. 1 982. B iological control of
insect pests. 4th Int. Isozyme Conj. New
York: Liss. In press
Knerer, G . , Atwood, C. E. 1973. Diprio­
nid sawflies: polymorphism and specia­
tion. Science 1 7 9 : 1 090--99
Krebs, C. 1 . 1 978 . Ecology: The Ex­
perimental Analysis of Distribution and
Abundance. New York: Harper & Row
Kreslavsky, A. G . , Mikheev, A. V . ,
Solomatin, V . M . , Grizenko, V. V .
1 9 8 I . Genetic exchange and isolating
mechanisms in sympatric races of Loch­
maea capreae (Coleoptera, Chrysomeli­
dae) . Zool. Zh. 60:62-68
Krysan , J. L . , Smith, R. F. , Guss, P. L.
1983 . Diabrotica barberi (Coleoptera:
Chrypomelidae) elevated to species rank
based on behavior, habitat choice, mor­
phometrics, and geographical variation
of color. Ann. En/omol. Soc. Am.
76: 1 97-204
Lacy, R. C. 1983. Structure of genetic
variation within and between populations
of mycophagous Drosophila. Genetics.
Submitted for publication
Levene, H . , Dobzhansky, T. 1959.
Possible genetic difference between the
head louse and the body louse. Am. Nat.
93: 347-5 3
Liquido, N. 1. 1978. Morphology, cytol­
ogy and breeding behavior ofNilaparva­
ta lugens (Stal) (Delphacidae, Homop­
tera) . MS thesis. Univ. Philipp . , Manila
Marshall, S . A . , Eymann, M. 198 1 . Mi­
cro-organisms as food for the onion mag­
got, Delia (Hylemya) Antiqua (Diptera:
Anthomyiidae). Proc. Entomol. Soc.
ant. 1 1 2: 1-5
Maugh, T. H. 1982. Exploring plant re­
sistance to insects. Science 2 16:722-23
Mayr, E. 1963. Animal Species and
Evolution . Cambridge, Mass: Harvard
Univ. Press
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
95. Mayr, E. 1970. Populations, Species,
and Evolution. Cambridge, Mass: Har­
vard Univ. Press
96. McClure, M. S . 1977. Population dy­
namics of the red pine scale, Matsucoc­
cus resinosae (Homoptera: Margarodi­
dae): the influence of resinosis. Environ.
Entomol. 6:789-95
97. McKenzie, J. A . , Parsons, P. A. 1974.
Microdifferentiation in a natural popula­
tion of Drosophila melanogaster to alco­
hol in the environment. Genetics 77:38594
98. Menken, S. B . J . 198 1 . Host races and
sympatric speciation in small ermine
moths, Yponomeutidae. Entomol. Exp .
Appl. 30:280-9 1
99. Merrell, D. J. 198 1 . Ecological Genet­
ics. Minneapolis: Univ. Minn. Press
100. Miller, D. R. , Kosztarab, M. 1979. Re­
cent advances in the study of scale in­
sects .
Ann.
Rev.
Entornot.
24:1-27
1 0 1 . Miller, J. R . , Strickler, K. L. 1983. In­
sect/plant interactions--Role of chemi­
cals in finding and accepting hosts. In
Chemical Ecology of Insects, ed. W .
Bell, R. Carde. I n press
102. Mitter, C . , Futuyma, D. J. 1979. Popula­
tion genetic consequences of feeding
habits in some forest Lepidoptera. Genet­
ics 92:1005-21
103. Mitter, C . , Futuyma, D. J. 1983 . An
evolutionary-genetic view of host-plant
utilization by insects. See Ref. 2a. In
press
104. Mittler, T. E. 1973. Aphid polymor­
phism as affected by diet. Bull. Entomol.
Soc. N.Z. 2:65-75
105. Miiller, F. P. 1976. Hosts and non-hosts
in subspecies of Aulacorthum solani
(Kaltenbach) and intraspecific hybridiza­
tions (Homoptera: Aphididae). In The
Host-Plant in Relation to Insect Behavior
and Reproduction, ed. T. Jermy. New
York: Plenum
106. Nielson, M. W . , Don, H. 1974. Interac­
tion between biotypes of the spotted alfal­
fa aphid and resistance in alfalfa. J.
Econ. Entomol. 67:368-70
107. Noble, W. B . 1 93 1 . Two wild grasses as
hosts of the Hessian fly, Phytophaga des­
tructor. J. Agric. Res. 42:589-92
108. Norris, D. M . , Kogan, M. 1980. Bio­
chemical and morphological bases of
resistance. InBreeding Plants Resistance
to Insects, ed. F. G. Maxwell, P. R.
Jennings, pp. 23-6 1 . New York: Wiley
109. Norris, D. M . , Rozental, J. M . , Sam­
berg, G . , Singer, G. 1977. Protein-sulfur
dependent differences in the nerve recep­
tors forrepellent 1 ,4- naphthoquinones in
two strains of Periplaneta americana.
Compo Biochem. Physiol. C 57:55-59
501
1 10. Orr, L. W . 193 1 . Studies on natural vs.
artificial control of the pine tortoise scale.
Univ. Minn. Agric. Exp. Stn. Tech . Bull.
No. 79
I l l . Ortega, A . , Vasal, S . K . , Mihm, J . , Her­
shey, C. 1980. Breeding for insect re­
sistance in maize. See Ref. 108, pp.
371-419
1 1 2 . Painter, R. H. 195 1 . Insect Resistance in
Crop Plants. New York: Macmillan
l B . Papaj , D . R. , Rausher, M . D . 1983. Indi­
vidual variation in host location by phy­
tophagous insects. See Ref. 55. In press
1 14. Pashley , D. P . , Bush, G. L. 1979. The
use of allozymes in studying insect move­
ment with special reference to the codling
moth, Laspeyresia pomonella (L.)
(Olethreutidae) . In Movement of Highly
Mobile Insects: Concepts and Methodol­
ogy in Research, ed. R. L. Rabb, G. G.
Kennedy, pp. 333-4 1 . Raleigh: N. C.
State Univ. Graphics
1 1 5 . Paterson, H. E. H. 198 1 . The continuing
search for the unknown and unknowable:
a critique of contemporary ideas on spe­
ciation. S. Afr. J. Sci. 77: 1 1 3-19
1 1 6. Phillips, P. A., Barnes, M. M. 1975.
Host race formation among sympatric ap­
ple, walnut, and plum populations of the
codling moth, Laspeyresia pomonella.
Ann. Entomol. Soc. Am. 68: 1053-60
1 17 . Plapp, F. W. Jr. 1983. Genetics of in­
secticide resistance. Pestic. Biochem.
Physiol. In press
1 1 8. Powell, J. R. 1983. Genetic and
nongenetic mechanisms of speciation. In
Mechanisms of Speciation, ed. C. Bari­
gozzi, pp. 67-74. New York: Liss
1 1 9. Powell, J. R. 1983. Interspecific cyto­
plasmic gene flow in the absence of nu­
clear gene flow: evidence from Droso­
phila. Proc. Natl. Acad. Sci. USA 80:
492-95
120. Price, P. W. 1980. Evolutionary Biology
of Parasites. Princeton: Princeton Univ.
Press
1 2 1 . Price, P. W . , Bouton, C. E . , Gross, P . ,
McPheron, B . A . , Thompson, J. N . ,
Weis, A . E. 1980. Interactions among
three trophic levels: influence of plants
on interactions between insect herbivores
and natural enemies. Ann. Rev. Ecol.
Syst. 1 1 :41-65
122. Price, P. W . , Willson, M. F. 1976. Some
consequences for a parasitic herbivore,
the milkweed longhorn beetle, Tetraopes
tetrophthalmus, of a host plant shift from
Asclepias syriaca to A . verticillata.
Oecologia 25:331-40
123. Prokopy, R . J . , Averill, A . L . , Cooley,
S. S . , Roitberg, C. A. 1982. Associative
leaming in egglaying site selection by
apple maggot flies. Science 2 1 8:76-77
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
502
DIEHL & BUSH
123a. Prokopy, R. J . , Avrill, A. L., Cooley,
S. S . , Roitberg, C. A . , Kallet, C. 1982.
Varialion in host acceptance pattern in
apple maggot flies. See Ref. 20,pp. 1 2329
124. Raffa, K. F., Berryman, A . A. 1982.
Physiological differences between lodge­
pole pines resistant and susceptible to the
mountain pine beetle and associated mi­
croorganisms. Environ. Entomol. 1 1 :
486-92
125. Rausher, M. D. 1982. Population dif­
ferentiation in Euphydryas editha butter­
flies: larval adaptation to different hosts.
Evolution 3:581-90
1 26. Reissig, W. H . , Smith, D. C. 1978.
Bionomics of Rhagoletis pomonella in
Crataegus. Ann. Entomol. Soc. Am. 7 1 :
1 55-59
127. Room, P. M . , Harley, K. L. S . , Forno, I .
W . , Sands, D. P. A. 198 1 . Successful
biological control of the floating weed
salvinia. Nature 294:78-80
128. Rosen, D. 1978. The importance ofcryp­
tic species and specific identifications as
related to biological control . See Ref. 2 1 ,
pp. 23-35
129. Rossiter, M. A . , Howard, D. J . , Bush,
G. L. 1983. Symbiotic bacteria of Rha­
goletis pomonella. See Ref. 45. In press
130. Rothschild, M . , Clay, T. 1952. Fleas,
Flukes, and Cuckoos-A Study of Bird
Parasites. New York: Philos. Lib.
130a. Russell, G. E. 1978. Plant Breedingfor
Pest and Disease Resistance. Boston:
B utterworths
1 3 1 . Salt, G. 1937. The egg-parasite of Sialis
lutaria: a study of the influence of the
host upon a dimorphic parasite. Para­
sitology 29:539-53
132. Salt, G . , Van den Bosch, R. 1967. The
defense reactions of three species of
Hypera (Coleoptera, Curculionidae) to
an Ichneumon wasp. l. Invertebr.
Pathol. 9 : 1 64-77
133. Saxena, R. C . , Rueda, L. M. 1982. Mor­
phological variations among three bio­
types of the rice brown planthopper Nila­
parvata lugens in the Phillipines. See
Ref. 20, pp. 435-36
134. Schneider, D . , Boppre, M . , Zweis, J . ,
Horsley, S. B . , Bell, T . W. , et al 1982.
Scent organ development in Creatonotos
moths: regulation by pyrrolizidine alka­
loids. Science 2 1 5 : 1 264-65
135. Schneider, W. D . , Miller, J. R . , Brez­
nak, J. A . , Fobes, J. F. 1983. Onion
maggot, Delia antiquo, survival and de­
velopment on onions in the presence and
absence of microorganisms. Entomol.
Exp. Appl. 33:50-56
136. Scriber, J. M. 1983. The evolution of
1 37 .
1 38.
1 39.
140.
141.
142.
143.
144.
145.
146.
147.
148 .
149.
150.
15 1 .
feeding specialization, physiological
efficiency, and host races. See Ref. 2a. In
press
Scriber, J. M. 1982. Food plants and
speciation in the Papilio glaucus group.
See Ref. 20, pp. 307-14
Shapiro, A. M. 1976. Seasonal Poly­
phenism. Evol. Bioi. 9:259-333
Shaposhnikov, G. Ch. 198 1 . Popula­
tions and Species in Aphids and the Need
for a Universal Species Concept. Ottawa:
Agric. Can.
Shimura, I. 1972. Breeding of chestnut
varieties resistant to chestnut gall wasp,
Dryocosmus kuriphilus Yasumatsu. lpn .
Agric. Res. Q . 6:224-30
Showers, W. B . 198 1 . Geographic varia­
tion of the diapause response in the Euro­
pean corn borer. In Insect Life History
Patterns: Habitat and Geographic Varia­
tion. ed. R. F. Denno, H . Dingle, pp.
97-1 1 1 . New York: Springer- Verlag
Simpson, G. G. 196 1 . Principles of
Animal Taxonomy. New York: Columbia
Univ. Press
Sims, S. R. 1980. Diapause dynamics
and host plant suitability of Papilio zeli­
caon (Lepidoptera: Papilionidae). Am.
Midi. Nat. 103:375-84
Singer, M . C. 1983. Determinants of
multiple host use by a phytophagous
insect population. Evolution 37:389403
Smith, H. S. 1941 . Racial segregation in
insect populations and its significance in
applied entomology. J. Econ. Entomol.
34: 1 - 1 2
Smith, M . A . , Cornell, H. V. 1979. Hop­
kins host-selection in Nasonia vitripennis
and its implications for sympatric specia­
tion. Anim. Behav. 27:365-70
Smith, R. H. 1977. Monoterpenes of
ponderosa pine xylem resin in western
United States. USDA For. Servo Tech.
Bull. No. 1532
Sogawa, K. 1982. The rice brown plant­
hopper: feeding physiology and host
plant interactions. Ann. Rev. Entomol.
27:49-73
Sosa, O. Ir. 198 1 . Biotypes I and L of the
Hessian fly discovered in an Indiana
wheat field. l. Econ . Entomol. 74:18082
Starmer. W. T. 1982. Associations and
interactions among yeasts , Drosophila
and their habitats. In Ecological Genetics
and Evolution . The Cactus-Yeast Model
System, ed. J. S . F. Barker, W. T. Star­
mer. New York: Academic:
Stock, M . W . , Amman, G. D . , Higby, P.
K. 1983. Genetic variation in mountain
pine beetle (Dendroctonus ponderosae) .
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
INSECT BIOTYPES
Populations from Seven Western States.
Ann. Entomol. Soc. Am. In press
152. Stock, M. W . , Castrovillo, P. J. 1 98 1 .
Genetic relationships among representa­
tive populations of five Choristoneura
species: C. occidentalis, C. retiniana, C.
biennis, C. /ambertiana, and C. fumi­
ferana (Lepidoptera: Tortricidae). Can.
Entomol. 1 1 3:857-65
15 3 . Stokes, B . M. 1957. Observations and
experiments on the Hessian fly (Maye­
tiola destructor Say). Ann. Appl. Bioi.
45 : 1 22-32
154. Stolz, D . B . , Vinson, S . B . 1977. Bacu­
lovirus-like particles in the reproductive
tracts of female parasitoid wasps. II: the
genus Apanteles. Can. J. Microbiol.
23:28-37
155. Sturgeon, K. B . , Mitton, J. B. 1982.
Evolution of bark beetle communities. In
Bark Beetles in North American Coni­
fers. ed. J. B . Mitton. K. B. Sturgeon.
Austin: Univ. Tex. Press
156. Tabachnick, W. J . , Powell, J . R. 1979.
A world-wide survey of genetic variation
in the yellow fever mosquito. Aedes
aegypti. Genet. Res. 34:21 5-29
157. Tabashnik, B . E. 1983. Host range
evolution: the shift from native legume
hosts to alfalfa by the butterfly, Colias
philodice eriphyle. Evolution 37: 1 5062
158. Tabashnik, B . E. 1983. Evolution of host
plant utilization in Colias butterflies. See
Ref. 24. In press
159. Tauber, C. A . , Tauber, M. J. 1 98 1 . In­
sect seasonal cycles: genetics and evolu­
tion. Ann. Rev. Ecol. Syst. 12:28 1-308
160. Tauber, C. A . , Tauber, M. J. 1982.
Evolution of seasonal adaptations and life
history traits in Chrysopa: Response to
diverse selective pressures . In Evolution
and Genetics of Life Histories. ed. H.
Dingle, J . P. Hegmann, pp. 5 1-72. New
York: Springer-Verlag
1 6 1 . Tavormina, S. J. 1982. Sympatric genet­
ic divergence in the leaf-mining insect
Liriomyza brassicae (Diptera: Agromy­
zidae) . Evolution 36:523-34
162. Taylor. C. E Powell. J. R. 1977. Mi­
crogeographic differentiation of chromo­
somal and enzyme polymorphisms in
Drosophila persimilis. Genetics 85 :68195
163. Thompson, W. R., Parker, H. L. 1927.
Host selection in Pyrausta nubilalis.
Hubn. Bull. Entomol. Res. 1 8:359-64
164. Thorpe, W. H. 1930. Biological races in
insects and allied groups. Bioi. Rev. 5:
177-21 2
165. Thorpe, W. H. 1939. Further studies on
pre-imaginal olfactory conditioning in in. •
503
sects. Proc. R. Soc. London Ser. B
1 27:424-33
166. Thottappilly, G . , Eastop, V. F . , Bath, J .
E. 1977. Morphological Variation within
Acyrthosiphon pisum and in ability to
transmit broad bean severe chlorosis
virus. Entomol. Exp . Appl. 22:29-34
167. Triantaphyllou, A. c. , Hirschmann, H.
1980. Cytogenetics and morphology in
relation to evolution and speciation of
plant-parasitic nematodes . Ann. Rev.
Phytopathol. 1 8 :333-59
168. Uvarov, B . 1966. Grasshoppers and Lo­
custs. A Handbook of General Acridolo­
gy. Vol. I . , Anatomy. Physiology. De­
velopment, Phase Polymorphism. Intro­
duction to Taxonomy. New York: Cam­
bridge Univ. Press
169. van de Water, T. P. M. 1983. Speciation
in the small ermine moth Yponomeuta
padellus L. (Lepidoptera, Yponomeuti­
dae) in Northern Europe. Neth. J. Zool.
In press
170. van Drongelen, W. 1979. Contact chem­
oreception of host plant specific chemi­
cals in larvae of various Yponomeuta spe­
cies (Lepidoptera). J. Compo Physiol.
1 34:265-79
1 7 1 . Vinson, S. B . 1 98 1 . Habitat Location. In
Semiochemicals-Their Role in Pest
Control. ed. D. A. Norlund, R. L. Jones,
W. E. Lewis. New York: Wiley
172. Von Laudien, H . , Iken, H. H. 1977.
Okologische Pragung und Protein­
biosynthese. Versuche mit Drosophila
melanogaster Meigen. Z. Tierpsychol.
44: 1 1 3-29
173. Wallace, B . 1 98 1 . Basic Population
Genetics. New York: Columbia Univ.
Press
174. Walsh, B.
1864. On phytophagic
varieties and phytophagic species. Proc.
Entomol. Soc. Philadelphia 3:403-30
175. Weis, A. E. 1982. Use of a symbiotic
fungus by the gall maker Asteromyia
carbonifera to inhibit attack by the para­
sitoid Torymus capite. Ecology 63: 16025
176. White, M. J. D. 1978. Modes o/Specia­
tion. San Francisco: Freeman
177. Wilson, A. C . , Maxson, L. R . , Sarich,
V. M. 1974. Two types of molecular
evolution, evidence from studies of in­
terspecific hybridization. Proc. Natl.
Acad. Sci. USA 7 1 :2843-47
178. Wilson, D. S. 1983. Genetic polymor­
phism for carrier preference in a phoretic
mite. Ann. Entomol. Soc. Am. 75:29396
179. Wilson, E. 0. 1 97 1 . The Insect Societies.
Cambridge, Mass: Harvard Univ. Press
180. Wood, D. L. 1982. The role of pher-
504
DIEHL & BUSH
Annu. Rev. Entomol. 1984.29:471-504. Downloaded from www.annualreviews.org
by University of Texas - Austin on 03/19/13. For personal use only.
omones, kairomones, and a1lomones in
the host selection and colonization be­
havior of bark beetles. Ann. Rev. En­
tarnal. 27:41 1-46
1 8 1 . Wood, T. K . , Guttman, S. I. 1983. En­
chenopa binotata complex: sympatric
speciation? Science 220:310-12
182. Yasumatsu, K. 1958. An interesting case
of biological control of Ceroplastes
rubens Maskell in Japan. l'roc. 10th Int.
Congr. Enloma!. 4:771-75
183. Zimmerman, M. 1982. Facultative de­
position of an oviposition-deterring pher­
omone by Hylemya. Environ. Entomol.
1 1 : 5 1 9-22
184. Zwolfer, H. 1983. Life systems and
strategies of resource exploitation in
Tephritids. See Ref. 45. In press