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Transcript
Animal Clones and Diversity
Are natural clones generalists or specialists?
Robert C. Vrijenhoek
A
sexual reproduction, or cloning, occurs naturally in most
animal phyla. Indeed, alternation between sexual and asexual
phases of the life cycle is relatively
common in some invertebrate taxa.
However, obligately (i.e., strictly)
asexual "species" are rare, comprising little more than 1 in every 1000
of the named animal species (White
1978). Biologists study these exceptions to the "rule of sex" for the
same reasons that medical scientists
probe disorders and diseases to define the limits of human health. Identifying the conditions in which
asexual lineages prosper or fail provides -a window through which biologists can view the adaptive significance of genetic diversity and sex.
The lessons to be learned from natural clones are particularly relevant as
an era begins in which the artificial
cloning of mammals, and potentially
humans, is no longer a fantasy.
To an evolutionary biologist, sex
is meiotic recombination· and outcrossing, which together create genetically diverse offspring that interact uniquely with the environment in
each new generation. Meiotic sex
originated in our single-celled protist ancestors, and except for the
evolution of distinct male and female gametes (i.e., small motile sperm
Robert C. Vrijenhoek (e-mail: [email protected]
ahab.rutgcrs.edu) is director of the Center
for Theoretical and Applied Genetics at
Rutgers University, New Brunswick, NJ
08903-0231. His interests are evolution,
population genetics, conservation, and
marine biology. © 1998 American Institutc of Biological Scicnces.
August 1998
Studies of animal clones
provide insight into the
ecological benefits of
genetic variability
and large eggs), the basic sexual
mechanism has changed little in the
evolution of multicellular plants and
animals. Nevertheless, the origins of
sex and factors that maintain such a
complex and costly process have been
hotly debated among evolutionary
biologists (Williams 1975, Maynard
Smith 1978, Bell 1982, Michod
1995). Perhaps clues to the benefits
of sex can be learned by studying
organisms that have abandoned this
process.
Obligately asexual lineages have
arisen naturally in most animal taxa
(with the exception of birds and mammals), and clones flourish in certain
environments. Nevertheless, individual
clones appear to be evolutionary dead
ends with limited adaptive potential.
Few obligately asexual taxa (with
the notable exception of bdelloid rotifers) have diversified to the point at
which a taxonomist would name new
species and genera (White 1978). A
low rate of diversification, coupled
with a high rate of extinction, may
explain why there are so few asexual
species (Stanley 1975). On the tree
of life, asexual animals represent little
more than a few twigs at the tips of
bountiful branches that are fundamentally sexual.
Apart from mutations, asexual
progeny are genetically identical to
their mothers. An asexual population may be composed of a single
clone whose genotype is essentially
constant across generations. At the
opposite extreme, random sexual
matings produce a nearly unlimited
array of genotypes and phenotypes
that differ in each generation. Most
natural populations lie somewhere
between these extremes. For many
sexual populations, nonrandom mating systems (e.g., inbreeding and assortative mating) and geographical
subdivisions can greatly increase genetic correlations among individuals
and between generations. Correspondingly, many asexual populations are composed of numerous ecologically different clones that arose
independently from diversified sexual
ancestors. Such diverse clones provide natural experiments that allow
biologists to study interactions between fixed genotypes and environments that vary in time and space.
In this article, I consider ecological factors that should favor such
clonally diverse specialized clones in
certain circumstances and a single
generalized clone in others. These
contrasts help to clarify the benefits
of genetic diversity and the processes
that generate it.
Models for clonal adaptation
Asexual organisms flourish in certain environments. Their success has
been attributed to a variety of factors, including reproductive efficiency, faithful replication of gen617
T
Modes of asexual reproduction in animals
o understand the ecology of clones, it is necessary to first consider some genetic, developmental, and
demographic consequences of asexual reproduction. Vegetative reproduction (fragmentation, fission,
and budding) circumvents egg production and is strictly somatic. Because the products of sexual reproduction, eggs and larvae (seeds in plants), often mediate the ecologically fundamental process of dispersal,
whereas vegetative reproduction does not yield such dispersal products, vegetative reproduction is more
properly considered a form of growth than of reproduction (Pearse et a1. 1989). Egg production in many
invertebrate animals (e.g., cladocerans, brine shrimp, aphids, rotifers, and digenetic trematodes) alternates
between sexual and parthenogenetic phases. From an evolutionary perspective, however, such cyclical
parthenogenesis is fundamentally sexual. However, some waterfleas (Daphnia) and brine shrimp (Artemia)
lose the sexual phase when obligately asexual lineages take over a population (Hebert 1981, Browne and
Hoopes 1990).
In a strict sense, parthenogenesis (virgin birth) involves only females (Figure la). Cytogeneticists have
identified a variety of mechanisms that mediate egg production in parthenogenetic animals (Suomalainen et
a1. 1987), but in the context of the adaptive value of clones, it is only relevant that these mechanisms produce
either completely homozygous
or permanently heterozygous
a. Parthenogenesis
b. Gynogenesis
c. Hybridogenesis
clones. Ameiotic (also known
as functionally apomictic)
parthenogens circumvent or
avert chromosomal recombiQ
...--nation (Mendelian segrega~~
tion, assortment, and crossI
I
ing-over) and transmit an
AS"
lO
intact
diploid (or, in many
- I ~
cases,
polyploid)
set of chroQ
..--~~
mosomes to their eggs. FuncI
I
tionally apomictic parthenogens typically have elevated
levels of heterozygosity, particularly in clones that arose
Figure 1. All-female modes of reproduction in animals. (a) Parthenogenesis, a strictly as hybrids. By contrast, meiall-female and clonal form of inheritance, is found in reptiles, insects, and many other otic parthenogenesis, which is
invertebrate taxa (but not in fish, although they are shown here for convenience). The functionally equivalent to selfgenotypes (AB) of parthenogenetic mothers and daughters are identical. (b) Gynogen- fertilization, leads rapidly to
esis, a form of parthenogenesis that requires sperm to initiate cleavage of eggs, occurs complete homozygosity. Some
in fish, amphibia, and a wide range of invertebrates. Genetic material from the sperm parthenogenetic Rhabditis
is not incorporated or expressed in the offspring. (c) Hybridogenesis, a hemiclonal form nematodes have normal meiof inheritance, occurs in a few fish, frogs, and insects. Only the maternal chromosome otic divisions and restore dipset (A) is transmitted to the eggs; the paternal set (B) is discarded during egg production.
loidy by fusing the haploid
In each generation, the eggs are truly fertilized by sperm from males of a sexual host.
egg
nucleus with a polar body
As this hypothetical example illustrates, paternal traits (fin spot in B' and tail crescent
in B") that segregate in the host population are expressed in the hybrids but are not nucleus. Complete homozygosity occurs in one step in some
transmitted through the eggs.
parthenogenetic Artemia-the
~
~~
~
~
~~
~
~
~
era I-purpose genotypes, and generation of specialized genotypes. Although certain hypotheses about
clonal adaptation may seem to be
contradictory, they are not necessarily so.
Geographical parthenogenesis.
Asexual organisms are found more
frequently at extreme latitudes, at
higher, altitudes, at the margins of a
species' range, on islands, and in
618
~~
0--
if
regularly disturbed communities, a
pattern commonly known as "geographical parthenogenesis" (Vande!
1928). Parthenogenesis facilitates
colonization of new habitats because
a single dispersing female can establish a new population. By contrast,
at least one male (or stored sperm)
and a female are needed to establish
a sexually reproducing population.
Sexual individuals face additional
handicaps finding mates when popu-
lation density is low, whereas colonizing parthenogens have" reproductive assurance" (Baker 1965). Consequently, all-female reproduction
endows parthenogens with at least
twice the net replacement rate of
sexual colonists, which devote half
of their progeny to males. Conversely,
some researchers argue that parthenogens are more abundant in peripheral environments because they
are inferior competitors in central
BioScience Vol. 48 No.8
Table 1. All-female biotypes of fish in the genus Poeciliopsis.
haploid egg nucleus is duplicated and identical meiN umber of
otic products are fused .
Reproductive mode
clones identiAbbreviation
Paternal host
fied to date
Biotype'
Regardless of the consequences (heterozygosity or
Gynogens (triploid)
homozygosity), a preP. 2 monacha-lucida
MML
P. monacha
3
P. monacha-2 Lucida
P. Lucida
MLL
3
sumed benefit of partheMLV
P. m onacha-Lucida-viriosa
P. viriosa
nogenesis is faithful repliHybridogens (diploid)
cation of the maternal
P. monacha-Iucida
ML
P. lu cida
15
genotype.
P. monacha-occidentalis
P. occidentalis
MO
9
Whatever the mechaP. m onacha-Iatidens
MLt
P.latidens
nism of parthenogenesis,
all-female (or unisexual)
' A biotype is a particular combination of genomes from the hybridizing sexual progenitors. For
reproduction provides an
example, P. 2 monacha-Iucida (or MML) has two chromosome sets from P. monacha and one
from P. Lucida.
obvious advantage in rapb"?" indicates biotypes that have not been investigated with either a ll ozymic or mitochondria l
idly growing populations.
DNA markers.
A parthenogenetic female
has a "twofold advantage"
over a corresponding sexual female, who allocates half of her reproductive potential to male offspring. If
all else were equal, a parthenogenetic lineage should rapidly replace its sexual counterparts; however, sexual
reproduction in fact predominates overwhelmingly in plant and animal taxa (Williams 1975, Maynard
Smith 1978). The critical assumption that "all else is equal" (e.g., fecundity, survival, and niche requirements) between sexual and asexual counterparts lies at the heart of this "paradox of sex." However, this
assumption may be fundamentally flawed. As I will discuss, animal clones can be ecologically diverse,
differing from one another and their sexual counterparts.
Many asexual taxa cannot exclude their sexual counterparts because the all-female forms need sperm
from sexual males to initiate zygotic development in parthenogenetic eggs. Consequently, sperm-dependent
parthenogens are forced to coexist, and possibly compete, with a "sexual host" species. Avariety of spermdependent parthenogenetic modes are found in animals (Beukeboom and Vrijenhoek in press); here I foc us
on two forms that occur in fish of the genus Poeciiiopsis (topminnows; family Poeciliidae). Gynogenesis is
a strictly clonal form of inheritance-sperm are needed to stimulate development of the zygote but do not
contribute to its genotype (Figure 1b). Hybridogenesis is a half-clonal (or hemiclonal) form of inheritancesperm and egg nuclei fuse and paternal genes are expressed in the offspring (Figure 1c), but only the maternal
genome is transmitted to the next generation .
The genus Poeciliopsis contains six unisexual biotypes that arose as hybrids between Poeciiiopsis
monacha and four other sexually reproducing species (Table 1) . The name of each biotype reflects the
numbers and kinds of complete chromosome sets contained in the hybrid . The three gynogenetic biotypes
transmit an intact triploid genome to their offspring. However, the diploid hybridogenetic biotypes transmit
only a haploid, non-recombinant, monacha chromosome set (i.e., a hemiclone) to their eggs. Each
hybridogenetic biotype mates with males of a different species and expresses traits from the host species.
Genetic surveys of natural populations revealed that these unisexual biotypes contain m ultiple clones (or
hemiclones) that arose through independent hybridization events (Vrijenhoek 1979). Much of the evidence
I provide for ecological differences among clones and their sexual relatives derives from long-term studies
of these remarkable fish (see also Vrijenhoek 1994).
areas of a species' range. For example, some asexual lizards appear
to be "fugitives" that have escaped
from direct competition with their
sexual relatives by favoring ecologically marginal habitats (Wright and
Lowe 1968).
Colonizing parthenogens may gain
an additional advantage over colonizing sexuals-namely, protection
against inbreeding depression during founder events (Vrijenhoek
August 1998
1985). For example, fish of the genus Poeciliopsis were eliminated
from an isolated headwater tributary of the RIO Fuerte in Sonora,
Mexico, when the stream dried during a severe drought. The tributary
was subsequently repopulated by fish
that had persisted near springs a few
hundred meters downstream. The gynogenetic colonists retained a high
level of heterozygosity because of
theif clonal reproduction. By con-
trast, the sexual colonists had lost all
detectable heterozygosity, a probable consequence of a series of founder events during the ·recolonization
process. The sexual colonists also
exhibited signs of inbreeding depression: an increased parasite load, decreased developmental stability, and
a diminished ability to compete with
the gynogens. "Heterozygosity assurance" provided the clones with a
strong competitive advantage that
619
Figure 1. GeoI •
metrical mean fitArithmetic mean, .to =iiL~ =0.50
,.,
ness in a tempoGeometrio:: mean _ 0.49
rally fluctuating
"
1\
l i
0,8
environment. The
i i i '
i i i \
solid and dashed
i \
i \
lines represent the
0.6 i
j\)\
\
fitnesses of two
f \
\ i\
---------------1 -----+ -..! '
hypotheticalgenotypes living in an
0.4
\\",! \ f \/
environment that
iii
\ !
ii
fluctuates ran0.2
\J
V
domly over time.
Fitnesses of the
two genotypes
fluctua te around
an arithmetic
Generations
meanofO.5 (dotted line). However, the geometrical mean fitnesses of the genotypes differ. The genotype that
fluctuates less (solid line) has a greater geometrical mean fitness (0.49) than the
genotype that fluctuates more widely (dashed line, 0.46). The low fitness values
have a greater affect on the geometrical mean than the high values. Formulas for the
arithmetic (x ) and geometric (x ) means are shown-x represents the fitness value
at interval i.
g
,
,
d
lasted more than 20 generations. until
genetic variability was restored to
the sexual population (Vrijenhoek
1989b). With the restoration of variability. the sexual population recovered its fitness and regained ecological dominance over the local clones.
However, sperm dependence limits the fugitive abilities of gynogens
and hybridogens (Beukeboom and
Vrijenhoek in press). Es,aping from,
or competitively excluding. the
sexual host (as almost happened in
the previous example) guarantees reproductive failure. Ultimately. a limited supply of sexual males and sperm
negates the twofold advantage of allfemale reproduction and prevents
gynogens and hybridogens from completely replacing their hosts (Moore
and McKay 1971), Consequently,
gynogenetic and hybridogenetic fish
have relatively limited ranges that
are encompassed by the geographical limits of their hosts. By contrast,
many parthenogens (e.g .• the cockroach Pycnoscelus surinamensis and
the geckonid lizard Lepidodactylus
luguhris) have extensive ranges that
are completely outside those of their
sexual relatives (Parker and Niklasson in press). Gynogens and hybridogens therefore cannot play the role
of fugitives.
General-purpose genotypes. There
have been numerous attempts to define the ecological niche of clonal
620
animals. One model holds that clones
perpetuate "general-purpose genotypes" that endow them with a wide
niche and broad ecological tolerances; another holds that they possess specialized genotypes with high
fitness in a limited range of environments. The General-Purpose Genotype (GPG) model grew from the
observation that many broadly distributed asexual weeds can tolerate a
wide range of environmental conditions (Baker 1965). It was more explicitly developed to explain the
broad geographical range of some
parthenogenetic animals (Parker et
aL 1977). Lynch (1984) argued that
selection in a temporally varying environment should favor general-purpose clones with the highest geometrical mean fitness (Figure 1). Such
clones will suffer smaller losses when
conditions are poor and should replace specialized clones with limited
tolerance of poor conditions.
Pboxinus eos-neogaeus, a gynogenetic minnow that arose as a hybrid of Pboxinus eos and Pboxinus
neogaeus, may be a general-purpose
clone. Schlosser et a1. (1998) compared niche relationships and physical tolerances of a single clone commonly found in northern Minnesota
with characteristics of its sexual progenitors. All of the minnows favored
the highly oxygenated waters of upland ponds, but the clone was more
abundant than the progenitors in
collapsed beaver ponds and streams.
which have a lower oxygen content .
The clone tolerates hypoxic stress
better than either of its sexual progenitors, and morphological evidence
suggests that it occupies an intermediate trophic niche. Schlosser et aL
(1998) hypothesize that the temporal and spatial unpredictability of
this environment favored a generalpurpose genotype that occupies a
broad intermediate niche and thereby
precludes the establishment of additional clones.
Only a few additional studies have
similarly examined the physiological and ecological breadth of an individual clone, and support for the
GPG model is mixed (Parker and
Niklasson in press). For example,
the wide geographical distribution
of many asexual plants is often cited
as support for the GPG model
(Bierzychudek 1985). However, several criteria should be met before invoking this model. First, the existence
of cryptic (i.e., hidden) clones must be
ruled out by an examination of appropriate genetic markers. The use of
allozymes and DNA fingerprints allowed Schlosser et al. (1998) to verify
the existence of a single Pboxinus eosneogaeus done, but many asexual taxa
have cryptic clones with substantial
differences in ecologically relevant
traits. Second, physiological tolerances of individual clones should be
tested under environmentally realistic conditions. Performance in the
laboratory does not necessarily translate into fitness in nature-witness
the mule. a robust animal on the
farm that is nevertheless sterile.
Finally. the wide geographical distribution of individual clones may
not be sufficient evidence for broad
physiological or ecological tolerances
because such clones might occupy a
narrow but universally available
niche. For example. some widespread
clones of dandelions. earthworms,
and cockroaches depend on human
transport and habitat disruptionnowadays. a cosmopolitan and abundant niche. Although fluctuating selection in a temporally unpredictable
environment should favor broadly
tolerant individuals. the present evidence for general-purpose clones of
animals is largely inferential. Nevertheless, general-purpose genotypes
are believed to arise by at least three
BioScience Vol. 48 No.8
means: hybridization and heterosis,
polyploidy, and mutations.
Hybrid clones and heterosis. The
strong associations between asexual
reproduction and hybrid origins in
the vertebrates and some insects have
suggested that cloning fixes hybrid
vigor (heterosis), which in turn confers broad ecological tolerance (Schultz
1971, White 1978). Some unisexual
organisms have broader tolerance to
physical stresses than their sexual
counterparts-for example, thermal
tolerance is enhanced in Poeciliopsis
monacha-lucida (Bulger and Schultz
1979), and P. eos-neogaeus and the
frog Rana esculenta have enhanced
resistance to hypoxic stress (Tunner
and Nopp 1979, Schlosser et al.
1998). But is their enhanced tolerance due to heterosis?
To address this question, my colleagues and I synthesized new
hybridogenetic strains of Poeciliopsis
in the laboratory (Wetherington et
al. 1987). On average, the synthesized hybrids were less viable than
nonhybrid offspring, and a majority
of the hybrids were sterile. All of the
fertile hybrids were spontaneously
hybridogenetic, however. Although
several of the new strains were comparable to the sexual progenitors in
several fitness-related traits (e.g.,
growth rate, early reproductive investment, and survival), none was
inherently better, and most were substantially worse. We found no support for the hypotheses that heterosis (or a general-purpose genotype)
is a spontaneous product of hybridity. By contrast, a study of laboratory-synthesized hybridogenetic
strains of Rana found faster growth
rates and greater survival in hybrid
larvae, on average, than -in the parental strains (Gutmann et al. 1994).
The mean body mass of the hybrid
frogs was lower at metamorphosis
than that of the parentals, however.
Without knowing the combined effects of growth rates, body mass,
and survival on lifetime reproduction and survival of these frogs, it
may be premature to conclude that
hybrid vigor in some traits also confers higher fitness. Again, the example of the mule is instructive.
In addition, laboratory studies revealed that some natural hybrid 0genetic strains of P. monacha-lucida
grow faster and survive longer than
August 1998
their sexual progenitors (Schultz and
Fielding 1989), but the differences
are not due to heterosis. This conclusion stems from comparisons among
laboratory-synthesized P. monachalucida strains.'-Some of the synthetic
hybridogens also were fast-growing,
but many grew more slowly, and all
were equally heterozygous (Wetherington et al. 1987). Differences
among the synthetic hybridogens
resulted from variance in the combining abilities of the monacha and
lucida genomes. The fast-growing
natural strains of P. monacha-lucida
represent "good combinations" that
have survived. Biologists must therefore exercise caution in making inferences about heterosis and fitness
from comparative studies of natural
clones and their sexual relatives. We
see only nature's successful clonesnot the failures that natural selection
quickly purges.
Instead of heterosis, the association between unisexuality and hybridization in the vertebrates may
result from hybrid dysgenesis, in
which hybridization between divergent species and populations leads to
disrupted meiosis and sterility
(Vrijenhoek 1989a). Clearly, hybrid
sterility results in selection for spontaneous "cytogenetic accidents" that
rescue egg production and restore or
retain diploidy. These accidents can
quickly become established ifcoupled
with all-female reproduction and a
concomitant twofold reproductive
advantage.
Polyploidy and general-purpose
clones. The majority of unisexual
vertebrates and insects are polyploids
(Suomalainen et al. 1987), and elevated ploidy has been linked to general-purpose genotypes. Triploid
clones of the waterflea Daphnia pulex
are more cold tolerant and occur at
higher latitudes than diploid clones
(Beaton and Hebert 1988). One possible explanation for polyploid superiority is that selection among
clones has fixed genomic combinations that express the best characteristic of each species in the hybrid.
Nevertheless, the association between asexuality and elevated ploidy
provides no better evidence for an
inherent superiority of polyploids
than the association with hybridization provides for hybrid superiority.
Indeed, the polyploid association
may also result from dysgenesis. Most
diploid organisms occasionally produce unreduced eggs, which, if fertilized, result in triploid progeny that
are typically sterile. Such events create another window of opportunity for
the selection of "cytogenetic accidents"
that can restore egg production.
Another explanation for the asso~
ciation between asexuality and polyploidy is that prior establishment of
parthenogenesis facilitates the elevation of ploidy because meiosis has
already been circumvented. Indeed,
triploid forms of Poeciliopsis arose
by adding a third genome to a diploid unisexual ancestor (Schultz
1969). For example, P. monachalucida-viriosa (3n = 72) added a viriosa genome (In ~ 24) to a diploid P.
monacha-Iucida ancestor (2n = 48).
Still, for most asexual polyploids we
do not know whether asexuality or
polyploidy came first. The enhanced
performance of some natural polyploids over their diploid counterparts may also be a product of selection among clones and fixation of
the best genomic combinations from
sexual ancestors, rather than of elevated ploidy itself.
Mutations and clonal evolution.
In theory, general-purpose genotypes
could arise within an asexual lineage
if mutation rates are sufficient (Lynch
and Gabriel 1983). The discovery of
ancient asexual taxa with numerous
divergent species would provide evidence for the potency of mutational
advance, but few taxa meet this requirement. The best known exception is the rotifer class Bdelloidea,
which contains more than 350
asexual species in 18 genera. Bdelloid
clones include enormous numbers of
individuals and may have pandemic
distributions. They probably avoid
extinction because they can form a
dormant stage when conditions are
poor and because they have excep~
tional dispersal abilities. Larger organisms, with more limited population sizes, are more likely to suffer
"mutational meltdown" (also known
as Muller's Ratchet). Meltdown occurs in asexual populations because
mildly deleterious mutations will
tend to accumulate and lead to a
progressive deterioration of fitness
as clones with low mutational loads
are lost by chance (Lynch et al. 1993).
Apart from the bdelloids, little
621
nists reaching an underexploited environment increase niche breadth
through behavioral plasticity (i.e.,
the within-phenotype component).
As population density and competition for resources increase, ecological breadth can expand again by
selection for genes that enhance plasticity, and by diversifying selection
on genetic variation that controls
Resources
After selection
the between-phenotype component
of niche breadth. Diversification is
Sexual population
~
Clone I
Clone V
~
slowed in sexual populations, however, because novel genotypes that
can effectively exploit marginal re--- "':
sources are reshuffled in each gen]
:
~:l
eration, and the majority of sexual
5
i~
__
_______________ L~:
__
offspring regress phenotypically to
the population's mean. Roughgarden
Resource distribution
suggested that cloning would be a
rapid way to freeze divergent genotypes responsible for the betweenFigure 2. The Frozen Niche·Variation model of clonal establishment. Although phenotype component of niche
originally developed to explain clones that arose from hybridization, the model also breadth and to resolve the conflict
applies to clones of nonhybtid origin (Weeks 1993). Resources are assumed to be
between diversifying selection and
uniformly distributed (dashed line), and the utilization functions of a sexual
recombination.
population and several clones are assumed to be normally distributed (solid lines)
According to the FNV model, rebut different in width. New clones (I through V) are frozen from the phenotypic
distribution of the sexual ancestors. Natural selection will fix clones that exploit current origins of clones can freeze
marginal resources and overlap minimally with the sexual progenitors. Simulation the between-phenotype component
studies revealed that clonal invasion of the sexual niche begins at its margins and of variation that exists in genetically
slowly progresses towards the center.
variable sexual progenitors (Figure
2). Interclonal selection subsequently
acts on this array of genotypes, fasubstantive evidence exists for truly enon in finite populations (Lynch et voring clones fhat have minimal niche
ancient and diversified asexual taxa a1. 1993) may explain the virtual overlap with established clones and
(Judson and Normark 1996). A absence of truly ancient clones of with the sexual progenitors. On a
local scale, this process will generate
hybridogenetic Poeciliopsis lineage vertebrates and arthropods.
an assemblage of clones that can
has persisted for at least 100,000
years, but this is young compared to Frozen variation. Most of the geno- successfully coexist with one another
the ages of related sexual species, typic diversity seen in asexual verte- and with the sexual progenitors. If
which have persisted for millions of brate, arthropod, and snail popula- individual clones have narrower
years (Quattro et al. 1992). Diver- tions arises from multiple origins of niches than the sexual population,
gence of mitochondrial DNA se- clones from sexual ancestors, rather then two predictions follow: first, a
q uences suggests that some asexual than from mutational accumulation single clone should have limited comsalamanders and clams may be sev- within asexual lineages (Crease et al. petitive impact on genetically varieral million years old, but the nuclear 1989, Avise et al. 1992, Dybdahl able sexual relatives (i.e., competigenomes associated with these "mito- and Lively 1995). Discoveries of such tion is asymmetrical); second, a
chondrial clones" may not be ancient. diversity in unisexual Poeciliopsis diverse array of specialized clones
Instead, their nuclear genomes ap- led me to propose the Frozen Niche- could eclipse the sexual niche and
pear to be refreshed periodically by Variation (FNV) model (Vrijenhoek competitively displace the progenitors.
the incorporation of new chromo- 1979,1984). This model grew from Comparisons of monoclonal (single
some sets from the sexual gene pool. ideas expressed by Roughgarden clone) versus multic10nal (many
Elevated ploidy may buffer against (1972) on the evolution of niche clones) populations of Poeciliopsis
the meltdown of asexual lineages breadth. He hypothesized that "eco- support these predictions (Vrijenbeca use adding a new genome from logical release" (i.e., an increase in hoek 1979).
Ghiselin (1974) had previously
the sexual gene pool can mask accu- niche breadth commonly found in
mulated genetic lesions (Suomalainen colonizing species faced with reduced suggested that a genetically diverse
et a1. 1987). Overall, however, clones interspecific competition) results sexual population should be more
with many genes and small popula- from changes in the within- and be- efficient than a single clone at extion sizes are more likely to decay tween-phenotype components of tracting resources from a heterogethan advance from mutations. The morphological and behavioral varia- neous environment (also known as the
rapidity of the meltdown phenom- tion. He suggested that the first colo- "Tangled Bank" model; Bell 1982).
Before selection
~
~=C
622
I
r------------------------------~------~
~~
!
BioScience Vol. 48 No.8
Consequently, sexual competitors
should be able to coexist with a clonal
assemblage, so long as the sexual
niche remains wider than the combined asexual niche (Case and Taper
1986). Evidence for asymmetrical
competition between sexual and
asexual forms is found in lizards,
frogs, and fish (Vrijenhoek 1979,
Case 1990, Semlitsch 1993). Perhaps the most compelling evidence
for the competitive superiority of
sexual diversity is found in geckonid
lizards on South Pacific islands
(Petren et aJ. 1993). A single gecko
clone dominated most islands until it
was competitively displaced by recent sexual invaders. A frozen niche
may be vulnerable in the face of
novel sexual invaders.
Another feature of the FNV model
is that clones lost through competition, mutational meltdown, or stochastic events can be replaced if new
asexual genotypes are periodically
frozen from sexual progenitors. If
new asexual lineages arise frequently,
a diverse assemblage of clones could
eclipse the sexual niche and cause
extinction of the progenitors. However, most animal taxa appear to be
resistant to the production of
clones-perhaps because sexual lineages that were prone to generating
clones were rapidly driven to extinction by the clones they produced
(Nunney 1989). Computer simulations of the FNV model (Weeks 1993)
revealed that if clones do not arise
too frequently, and if natural resources are distributed uniformly,
then clones that exploit marginal resources will be favored over clones
that compete more directly with the
sexual population (Figure 2). Clones
with "marginal" phenotypes compete with smaller numbers of sexual
individuals that are generated in the
tails of the phenotypic distribution.
Clones with "central" phenotypes
may be capable of outcompeting
sexual individuals at the center of
the resource distribution, but "centralized" sexual phenotypes are regenerated in each generation by recombination. These simulations
produced results that are consistent
with the overall pattern of geographical parthenogenesis-clones are more
frequent in marginal environments.
A similar pattern exists on a microhabitat scale with unisexual
August 1998
Poeciliopsis (Vrijenhoek 1984). In
populations composed of a single
clone, the unisexual inividuals are
most abundant in peripheral pools,
and they are nearly absent in mainstream areas~ with some current,
where the sexual" individuals dwell.
In multiclonal populations, the unisexual fish completely dominate
pools and mainstream areas. In
cion ally diverse populations, unisexual females greatly outnumber the
sexual females and would probably
replace them altogether if sperm did
not become limiting for these
hybridogenetic fish.
The main assumption of the FNV
model is that clones can freeze variation that exists in the gene pool of
the sexual progenitors. We tested
this assumption by examining laboratory-synthesized hybridogenetic
strains of Poeciliopsis. The differences in morphology, physiology,
life-history traits, and behavior observed among these strains clearly
demonstrate the potential for freezing ecologically relevant phenotypic
variation (Schultz and Fielding 1989,
Wetherington et al. 1989b, Lima and
Vrijenhoek 1996, Lima et aJ. 1996).
Identifying similar differences among
natural clones of Poeciliopsis has
been a focus of our research efforts
during the past 25 years (reviewed
by Schultz and Fielding 1989, Vrijenhoek 1990). Recent studies of lizards, frogs, snails, brine shrimp, and
cladocera provide further evidence
for ecological diversification among
naturally occurring clones (Browne
and Hoopes 1990, Case 1990, Weider
1993, Jokela et a!. 1997, Semlitsch et
al. 1997). I focus the remaining discussion on recent studies of unisexual
fish. In particular, I examine hypotheses that unisexual organisms
of hybrid origin tend to occupy an
intermediate niche and that individual clones are phenotypically inflexible.
Hybrid clones and an intermediate niche. Moore (1977) expressed
an alternative view of clonal adaptation, hypothesizing that unisexuals
of hybrid origin can escape direct
competition with their sexual progenitors by occupying an intermediate niche. The gynogenetic minnow
clone (Phoxinus eos-neogaeus) found
in northern Minnesota is believed to
occupy such an intermediate niche
because its feeding structures are
generally intermediate (in a multivariate sense) to those of its progenitors, P. eos and P. neogaeus (Schlosser
et al. 1998).ltis a mistake, however,
to assume that fish hybrids invariably express intermediate phenotypes
(Ross and Cavender 1981). As Haldane (1932) noted, hybridization
"may merely lead to new combinations of the characters of the species
or groups which hybridize, but ... it
may also produce something entirely
fresh." For example, the laboratorysynthesized hybridogenetic strains of
Poeciliopsis monacha-Iucida were
broadly intermediate to the progenitors for most quantitative traits, but
several strains possessed phenotypes
that deviated greatly from the intermediate mean (Wetherington et al.
1989b, Lima and Vrijenhoek 1996,
Lima et al. 1996). In these cases,
behaviors and pigmentation patterns
were as extreme as the parental forms
(i.e., the hybrids expressed dominant phenotypes). If an uncontested
intermediate niche exists between
hybridizing sexual progenitors, selection will probably fix a clone with
the appropriate intermediate traits.
In this sense, Moore's (1977) hypothesis of an intermediate niche for
unisexual hybrids represents a special case of frozen niche-variation.
However, ecological intermediacy is
not an inevitable consequence of hybridization, as I shall discuss later.
It may also be a mistake to assume
that niche position is correlated with
morphology. For many species, behavioral plasticity plays a greater role
than morphology in determining the
use of food and spatial resources. For
example, natural hemiclones of Poeciliopsis monacha-lucida are broadly
intermediate to P. monacha and P.
lucida for the number of inner teeth
on the dentary bone (Figure 3). These
tiny teeth also occur on the premaxillary and pharyngeal bones, where
they produce an abrasive surface that
helps the fish to manipulate and swallow insect larvae. Although two P.
monacha~Jucida hemiclones, designated MLiVII and MLlVIII, both
have intermediate numbers of these
teeth, they differ greatly in predatory efficiency. Hemiclone MLIVII
is intermediate in its prey-handling
ability, and its natural diet is also
broadly intermediate (Weeks et al.
623
Figure 3. Dentition and preda- a
tion efficiency in
sexual and hybridogenetic biotypes of Poeciliopsistoprninnows
from the Arroyo
de Jaguari (Rio
Fuerte, Sonora,
P.lucida
Mexico). (a) The
P. monacha
left dentary bone
is illustrated for
each biotype
P. monacha-Iucida
{modified after b
4.5
Vrijenhoek and
Schultz 1974}.
(b) Relationships
between the mean
u
number of inner
! 4.0 P.lucida
teeth on the left
•E
dentary bone and
MLNII
handling time
(the mean time
MLNIII
between attacking and swallowP. monacha
ing chi rona mid
larvae; original
3.0 +--r--'--~-'----'-~-~~r--'--,
data from Weeks
20
40
60
80
100
et al. 1993). ErNumber
of
teeth
ror bars represent
one standard error on either side of the mean. The P. monacha-lucida biotype includes two hemiclones,
MLiVII and MLlVIII.
+
+
~
+
1992). If MLlVlI were the only unisexual fish found in its native stream,
it might be considered evidence for
the hypothesis of an intermediate
unisexual niche. However, it coexists with hemiclone MLIVIII, which
is a more efficient predator than either of its sexual progenitors. Thus,
the intermediate trophic morphology of MLIVIII does not constrain
this fish to an intermediate diet.
As the abundance of various kinds
of food changes seasonally, these fish
correspondingly shift their diets;
however, the degree of dietary plasticity differs greatly among the members of this fish assemblage. One
sexual species, P. lucida, is relatively
rigid in its feeding behavior-it is a
bottom-feeding detritivore. The other
sexual species, P. monacha, is more
flexible-it is the most herbivorous
member of this assemblage during
the dry season and the most predaceous following the rainy season,
when insect larvae are abundant.
Hemiclones MLlVlI and MLlVIII
both obtain intermediate quantities
of insects when larvae are abundant,
624
+
but when larvae are scarce, MLIVII
increases its herbivory and MLIVIII
becomes more predaceous. In the
laboratory, MLIVIII is an aggressive
predator that interferes with the foraging of other fish in this assemblage, often stealing insect larvae
from fish that are less efficient at
handling prey. Consequently, as
Haldane suggested, hybridization
appears to have resulted in something that is "entirely fresh" and not
seen in either of the parental species.
Phenotypic plasticity. Baker
(1965) suggested that plasticity in
some characters may be required to
stabilize fitness in a variable environment. Developmental plasticity
appears to be a common characteristic of widely distributed weeds and,
presumably, of general-purpose
genotypes. For example, some Daphnia species develop protective spines
when raised in the presence of predators. In contrast, phenotypically rigid
genotypes are expected to show
greater variance in fitness across fluctuating environments and should,
therefore, be subject to a higher rate
of extinction. Consequently, natural
selection should favor mutations that
increase the adaptive plasticity of
clones and lead to the evolution of
general-purpose genotypes (Lynch
1984).
Alternatively, cloning could freeze
the capacity for phenotypic plasticity from variation in the sexual progenitors, as demonstrated by the
laboratory-synthesized hybridogens
of Poeciiiopsis (Wetherington et al.
1989a). All of the synthetic strains
grew more slowly when reared on a
low-protein diet. This finding alone
is not surprising, but one strain suffered substantially less than the others.1t was the slowest-growing clone
when raised on a high-protein diet
and the fastest-growing clone when
raised on a low-protein diet. Such a
clone might suffer the least during
poor conditions and consequently
have the highest geometric mean fitness in a fluctuating environment.
However, these synthetic hemiclones
do not exist in nature. It seems likely
that natural clones froze similar life
history differences from variation in
the sexual ancestors (for examples,
see Schultz and Fielding 1989).
The capacity for phenotypic plasticity could be frozen because clones
are genotypes. involving thousands
of interacting genes that affect complex mixtures of traits. The rigid
dentition and plastic feeding behavior
of hemiclone MLIVIII illustrate this
complexity. Studies of the laboratorysynthesized hybridogens revealed
that complex feeding behaviors encompassing the range expressed by
natural hemiclones MLIVII and MLI
VIII could be frozen from the gene
pools of the sexual progenitors (Lima
1998). As biologists continue to study
clonal organisms from a multivariate ecological perspective, some
clones will likely turn out to be food
generalists and habitat specialists,
some will be food specialists and
habitat generalists, and some will be
specialists or generalists for both food
and habitat. Plasticity may be favored in traits that interact with seasonally varying resources , and rigidity may be favored in traits that
reduce interspecific competition. The
gene pools of sexual species such as
P. monacha store the historical solutions to all of these contingencies.
The clonal forms that this species
BioScience Vol. 48 No.8
has spawned freeze this in1.0
formation and use it to great
.----------.
... MMUI
effect during the short term,
because they numerically
O.B
dominate the fish communi\
ties in rivers in which recur~
.~
0-.
.
.
\
rent origins of new clones
0.6
,-----'-- ............ \
w
are possible (Vrijenhoek
0
~
P. monacha
1979). Clonal diversity that
\
is periodically frozen from
~~ 0.'
\
the sexual gene pool may be
a:
\
similarly responsible for the
MMUII
0.2
ecological success of many
asexual taxa. If this hypothesis is true, it may be hard to
0.0
~--------,--------,--escape the conclusion that a
Heat
Cold
Hypoxia
little sex (i.e., the generation
Type of stress
of novel recombinant genotypes) is also good for asexual
taxa (see also Green and Figure 4. Relative rates of survival under three kinds of
environmental stress in a sexual species and two hybridogenetic
Noakes 1995).
stress only, we might have
concluded that clone MMLI
11 is a broadly tolerant, general-purpose genotype. Its
wide distribution in several
headwater tributaries of the
Rios Fuerte and Sinaloa is
consistent with this interpretation. If, on the other hand,
we had studied hypoxic
stress only, we might have
concluded that MMLlII is
narrowly adapted. Clone
MMLIII also has narrow
feeding behavior-it is a
"drift feeder" that prefers to
feed on suspended prey items
found in shallow areas with
some current (Schenck and
Vrijenhoek 1989). Clearly,
MMLIII is a complex mixbiotypes of Poeciliopsis. The relative surviVal value equals the ture of generalist and speFitness variation in time and mean survival rate of each type of fish divided by the maximum cialist traits. In many resurvival rate (from Vrijenhoek and Pfeiler 1997).
space. Several recent studies
spects, the corresponding
of unisexual lizards, brine
clone, MMLII, appears to be
shrimp, snails, fish, frogs, and water- tolerance, feeding behavior, habitat more specialized-it has narrow therfleas have attempted to test predic- preference, and other characteristics. mal tolerances and a restricted range
tions of the GPG and FNV models as Researchers may reach erroneous in the Rio Fuerte. However, it is the
if they were mutually exclusive alter- conclusions about clones if they ex- most tolerant of these fishes to hynatives (Browne and Hoopes 1990, amine only a few traits. A recent poxic stress, and its feeding and
Weider 1993, Bolger and Case 1994, study of two gynogenetic clones swimming behaviors are least afJokela et a1. 1997, Semlitsch et a1. (MMLII and MMLlII of Poeciliopsis fected by the presence or absence of
1997, Schlosser et al. 1998). How- 2 monacha-lucida) that coexist in water currents (Schenck and Vrijenever, the two models do not neces- springs and streams of southern hoek 1989, Vrijenhoek and pfeiler
sarily lead to alternative predictions, Sonora, Mexico, illustrates this point. 1997). The behavioral and physibecause they are based on different Flash floods scour Sonoran streams ological complexity of these fishes
assumptions about environmental during the rainy season, and large suggests that claims about "generalheterogeneity in time and space. portions of the streambeds are with- ist" or "specialist" clones that are
Simple contrasts of these models as- out water during the long dry season based on studies of only a few traits
sume that fitness variation in time in this arid region. Consequently, should be made cautiously.
Perhaps the most significant lesshould favor general-purpose geno- some fish must survive in stagnant
types, whereas heterogeneity in food residual pools in which water tem- son to emerge from our studies is
and in spatial resources should favor peratures exceed 40°C and dissolved that the sexual species, P. monacha,
multiple specialized clones. As dis- oxygen concentrations drop to le- may be the most generalized of the
cussed above. most studies of thal levels. Other fish survive in three fishes. It has the broadest diet
multiclonal populations of unisexual springs and seeps, or in shady pools (Schenck and Vrijenhoek 1989) and
lizards, brine shrimp, snails, frogs, and crevices. During cold winter the best ability to tolerate shifts in
and waterfleas have supported the mornings, most fish are torpid, environmental stresses. Although P.
FNV model, and a study of mono- whereas others swim actively near monacha is not the best at surviving
clonal populations of Phoxinus eos- the effluents of natural hot springs. heat, cold, or hypoxic stress (Figure
neogaeus was consistent with the We tested the tolerance of the two 4), it is generally not the worst. Its
GPG model. Considering the evi- clones and their sexual host, P. tendency to be intermediate is a condence given below, however, even monacha, to heat, cold, and hypoxic sequence of averaging the survival
the Phoxinus example may not be stress (Vrijenhoek and Pfeiler 1997). differences across many genotypiNo single type of fish outperformed cally unique individuals (Vrijenhoek
inconsistent with the FNV model.
Predictions based on the GPG and the others across all three stresses (Fig- etal.1992). Consequently, the sexual
FNV models are confounded in natu- ure 4 )--clone MMLlII had the highest species may have the highest georal environments that vary in both survival rate during heat and cold metrical mean fitness in these seatime and space. As I have argued, stress, MMLII was best at surviving sonally and spatially heterogeneous
natural clones are complex mixtures hypoxic stress, and P. monacha gen- desert streams. The two clones, on
the other hand, are fixed genotypes
of specialized and generalized traits erally was average.
If we had studied heat and cold that exhibit much greater variance in
affecting life history, physiological
"
Y
'\--0
•
August 1998
625
survival across these stresses. Although the clones have highly elevated levels of heterozygosity (as a
consequence of their hybrid origins),
they do not appear to have broadly
enhanced physiological tolerances.
The wide fluctuations in survival of
the two clones result in lower geometrical mean fitnesses.
Clonal limits and
the benefits of sex
Genotypic and phenotypic differences among individuals are the essence of sexual reproduction and may
be required for species locked into
coevolutionary struggles with rapidly evolving biological enemies. The
Red Queen in Lewis Carroll's
Through the Looking Glass advised
Alice that "it takes all the running
you can do, to keep in the same
place." Genetic diversity is essential
for keeping up with parasites and
pathogens that evolve rapidly to exploit the most common host phenotypes. Rare host phenotypes may
escape infection and thereby gain a
temporary advantage until they too
are abundant and become the focus
of coevolving parasites. This cycle of
frequency-dependent fitness preserves genetic diversity in the host
population and favors the maintenance of sex (Hamilton et al. 1981).
Consequently, highly abundant
clones in a mixed reproductive complex should be more heavily parasitized than the unique individuals that
make up a sexual lineage. Support
for the Red Queen model has been
found in several studies of cion ally
reproducing animals, including
Poeciliopsis (Lively et al. 1990).
Many biologists believe that the Red
Queen model provides one of the
most powerful ecological explanations for the maintenance of sex and
genetic diversity in higher organisms
(Ridley 1993).
Ultimately, clones are fixed genotypes with limited abilities to respond to ca pricious biotic and physical environments. Natural selection
acts on the aggregate of gene interactions in clones, rather than the average effects of independent genes, as
in sexual species. Naturally occurring clones are successful genotypes
that involve the collaboration of
thousands of genes. Interactions be626
tween these clones and a variable
environment may be rigid for some
traits (e.g., morphology) and plastic
for others (e.g., behavior). Certain
clones are generalists along some
niche dimensions and specialists
along others. Although the gynogenetic fish clone MMLIII comes closest, we have found no truly multidimensional, general-purpose genotype
among clones of Poeciliopsis. The
divergent clonal lineages studied to
date represent only a small fraction
of the genotypic combinations that
have resulted from hybridization and
polyploidization events in this fish.
Natural selection rapidly purges the
bad genotypic combinations and preserves clones with compatible combinations.
The clonal diversity that is seen in
natural Poeciliopsis populations urtdoubtedly represents a biased subset
of genotypes that have passed this
first test of natural selection. However, even the good combinations
must be lucky enough to find an
uncontested niche. Clonal invasion
of a sexual population appears to
begin at the weakly contested margins of its ecological niche (Weeks
1993). Some unisexual taxa that
arose as interspecific hybrids may
occupy a weakly contested intermediate niche between their sexual progenitors; however, hybrids are not
necessarily intermediate for all characteristics, as exemplified by the
predatory efficiency of hemiclone
MLIVIII and the thermal tolerance
of clone MMLlII.
The GPG model predicts that environmental fluctuations will favor
the most broadly tolerant genotype
(Lynch 1984); nevertheless, asexual
populations often contain multiple
clones. How can this apparent contradiction be resolved? Perhaps genetic models provide an inadequate
view of clones. It may be more appropriate to view clones as we view
species in a biological community,
rather than as genes in a gene pool.
Community ecologists argue that intermediate levels of environmental
disturbance can facilitate the maintenance of species diversity (Connell
1978), and modeling studies reveal
that intermediate levels of disturbance can facilitate the maintenance
of clonal diversity if clones differ in
competitive abilities and reproduc-
tive rates (Sebens and Thorne 1985).
A promising experimental study
with Daphnia clones supports these
basic predictions (Weider 1993). Intermediate levels of disturbance
maintained the greatest diversity of
Daphnia clones, whereas high and
low levels of disturbance resulted in
less diversity. Long-term studies of
these clones are needed to identify
the specific tradeoffs between the
reproductive rates and competitive
abilities of clones. Nevertheless, a
pioneering study of dandelions
(Taraxacum officina/e) provides a
model for clonal coexistence under
intermediate disturbance (Sol brig
1971). One dandelion clone (A) matures early and produces more seeds,
whereas the other clone (D) is a superior competitor at high densities.
Without disturbance, clone D always
outcompetes clone A. With constant
disturbance, such as mowing or grazing, competitive abilities are unimportant, and clone A can win. Sol brig
(1971) hypothesized that the clones
can coexist because intermediate levels of disturbance favor each clone at
different times and in different places.
It would be relatively easy to maintain such clones with dispersal among
patches in a temporally and spatially
heterogeneous environment.
Over the long term, however, it
may not be important for a particular
genotype to be the best competitor or
to have the greatest reproductive
output in a particular environment,
so long as it is not often the worst
genotype in alternative environments. Unlike cloning, sex is not an
efficient way to consistently produce
the most fit genotype in a predictable
environment, but it avoids consistently producing the worst genotype
when conditions inevitably change
(Vrijenhoek and Pfeiler 1997). The
average, yet flexible, abilities of P.
monacha (the matriarchal ancestor
of all Poeciliopsis clones) to survive
opposing environmental stresses may
provide this species with the highest
geometrical mean fitness in its temporally and spatially varying habitats. Sexual species of Poeciliopsis
persist for many millions of years,
and their evolutionary longevity may
be a consequence of phenotypic regression that slows the adaptive response to fluctuating selection pressures and thereby avoids a higher
BioScience Vol. 48 No.8
probability of extinction suffered by
fixed genotypes (Eshel and Feldman
1970). Genetic variability in P.
monacha also plays a critical role in
its ability to live with parasites (Lively
et al. 1990), which probably contribute more than the physical environment to fluctuations in fitness
and the direction of selection.
Clonal organisms are natural evolutionary experiments. One of the
most valuable lessons learned from
these experiments is that clones can
freeze and faithfully replicate genotypic differences that exist in sexual
populations. Studies of natural and
laboratory-synthesized clones expose
the extraordinary variability that
exists in gene pools of sexual species.
The persistence of sexual progenitors faced with competition from allfemale clones supports the hypothesis that genotypic diversity provides
ecological benefits that can compensate for the costs of sex (Williams
1975). Meiosis and outcrossing may
also provide direct genetic benefits,
such as enhanced repair of mutations and "'rejuvenation" of the genome (Michod 1995). Evidence for
the immediate genetic benefits of sex
may be difficult to obtain in studies
of natural populations. but the possibility of such benefits warrants serious experimental investigation before we embark on the wholesale
cloning of mammals.
Acknowledgments
I thank my former students and colleagues who helped sample fish in
Mexico and rear strains so diligently
in the laboratory. Mostly, I thank R.
J. Schultz, who pioneered studies of
unisexual Poeciliopsis and stimulated
many of the studies summarized
herein. The research was funded
(1974-1992) by grants from the
National Science Foundation and the
New Jersey Agricultural Experiment
Station.
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