Download 122. Woodruff, D.S. and G.A.E. Gall. Genetics and conservation. In

122.
Woodruff, D.S. and G.A.E. Gall.
Genetics and conservation. In: Integrating Conservation Biology and Agricultural
Production. Special Issue of Agriculture, Ecosystems and Environment 42:53-73.
(1992c).
BOOK
CHAPTER
A~
53
Genetics and Conservation
DAVID S. WOODRUFF
1
J
I and
GRAHAM A.E. GALL2
Depanment of Biology, University of California, La Jolla, CA 92093 (U.S.A.)
Depanment of Animal Science, University of California, DOI'is, CA 95616 (U.s.A.)
ABSTRAcr
Woodruff. D.S. and Gall, G.A.E., 1992. Genetics and conservation. Agric. Ecosystems Environ., 42:
53-73.
The basic sciences of genetics and ecology have long played a vital role in agriculture. New
technologies spawning a gene revolution promise to revolutionlze agricultural genetics. The Opportunities
to utilize these new techniques, along with standard methods of animal and plant breeding, are great for
agriculture, conservation biology, and their synergism. Biological diversity is inextricably linked to human
welfare. Genetic engineering is viewed as having both promise and risk to agricultural and natural
biological systems, suggesting that its application must be evaluated on a case·by-case basis. In order to
adequately manage genetic resources, panerns of genetic variation must be documented and their
relationship to the life-histories of species and the functioning of ecosystems understood. To achieve this
goal, species to receive attention must be prioritized, possibly based on their usefulness as indicator species
in defining genetic management strategies for biological groups of species. Particular attention should be
given to invasive species, to the phenotypic plasticity of species, and the organizational complexity of
populations, communities, and ecosystems. A return to greater scientific emphasis at the organismal and
ecosystem level obviously is essential.
INTRODUCTION
There are a variety of ways the basic sciences of genetics and ecology
and their associated technologies can be applied to the problems faced by
agriculture and conservation. It is these biological basics that have sustained
life on the planet for three billion years. And there is every reason to
believe that their rigorous incorporation in the future can alleviate many
problems that, from this perspective, are so overwhelming.
This paper examines the complex interplay of genetics, conservation, and
agriculture in a hierarchical fashion, commencing with molecules and
proceeding to population, species and ecosystem levels of complexity. New
and extraordinarily promising biotechnologies are identified as are some of
the old, but sometimes ignored, lessons of basic genetics and ecology. It is
this holistic approach that promises to mark a gene revolution, which is just
beginning, as the most significant of agriculture'S three great transitions. The
post-glacial agricultural revolution relied heavily on the application of simple
54
genetic principles to the process of domestication. The dramatic green
revolution involved the application of more genetics and petrochemicals to
maximize short-term productivity in a handful of species. The gene
revolution promises far more sophisticated genetic manipulations, coupled
with the development of agricultural systems of much greater ecological
sensitivity. But from the outset, it is important to stress that genetic
technology alone does not offer a solution to the dilemma now facing both
agriculture and conservation biology.
There is a commonly held belief that biological diversity is inextricably
linked to human welfare. Biological diversity refers to the variety and
variability among living organisms and the ecosystems in which they interact.
Such diversity has evolved over a billion years and is responsible for
ecological processes which sustain all life, including that of our own recently
arrived species.
The number of species is large with some scientists suggesting that as
many as 30 million may exist. At the global level, the number of plants and
vertebrate animals are relatively well known, but the number of insect
species can only be guessed at, and other invertebrates probably number in
the hundreds of thousands (Table 1). Consequently, it is difficult to estimate
extinction rates, but it is agreed that loss of species is occurring at a very
high rate (McNeely, 1990). Agriculture utilizes only a few of these species,
but as the major user of land, it places pressure on species survival, and can
and must contribute to their conservation.
At the ecosystem level there is a growing realization that the conservation of landscape diversity is even more important in simplified agricultural
systems than in the natural ones they replaced. Losses of habitat and habitat
diversity cause species extinctions locally and affect climates and biogeochemical cycles over wide areas. Global agricultural productivity is
directly threatened by ongoing losses of ecosystem diversity, especially in the
tropics. Overviews of conservation at these higher levels of biological
organization are offered by Soule (1986) and Wilson (1988).
The current rate of reduction in biological diversity because of human
activities is a direct and serious threat to human welfare. To underscore the
importance of conserving biological diversity consider the following examples
of agricultural importance.
Mechanized harvesting of tomatoes was
facilitated by a gene for a jointless fruit stalk. Introduction of the gene into
cultivars made it worth millions of dollars annually. In nature, the gene
occurs only in a single population of a related species of tomato unique to
the Galapagos Islands. A single gene from Ethiopia protects California's
barley crop, worth $150 million a year, against yellow dwarf virus disease.
The majority of grapes in agricultural production in the world owe their
'2.."2..'2..
55
TABLEt
Summary of current state of knowledge concerning numbers of described species
Group
Bacteria and blue-green algae
No. species
4,760
Fungi
46,983
Algae
26,900
Bryophytes (mosses and liverworts)
17,000
Gymnosperms (conifers)
Angiosperms (flowering plants)
750
250,000
Protozoans
30,800
Sponges
5,000
Corals & Jellyfish
Roundworms and earthworms
9,000
24,000
Crustaceans
38,000
Insects
751,000
Other arthropods and minor invertebrates
Molluscs
132,461
Starfish
I
50,000
6,100
Fishes (teleosts)
19,056
Amphibians
4,184
Reptiles
6,300
Birds
9,198
Mammals
4,170
1Taken from MeNeel)' et al, (1990).
existence to the genetic endowment of a native species, Virus calif amicus, a
fact which 'illustrates the importance of multiple gene effects.
Examples of the importance of biological diversity at the level of species
and ecosystems for other California species come to mind. California sea
otters, though undeniably predatory to shellfish populations, have important
positive effects on kelp beds and their associated finfish populations and on
the enhancement of the local tourist industry. In California, as elsewhere, no
economic value is given to fish populations in evaluating most water project
developments. Consequently, salmon and steelhead trout populations have
declined dramatically. Proper management of these species and partial
restoration of the associated fisheries is estimated to yield a statewide
benefit of $150 million annually. The societal cost of destruction of riparian
woodlands and coastal wetlands in California has never been computed. But
56
the impact of resource mismanagement on potential agricultural productivity
must be enormous. Such diverse ecosystems played significant roles in
providing flood control, shoreline protection, fish and wildlife habitat, and
natural nutrient cycling at vastly superior rates to those occurring in the
agricultural systems that replaced them.
In each of these cases a cash value can be placed on the sustainable
return to conserving biological diversity. Furthermore, in each case some
element of diversity, or its utility, or its intrinsic value, involves an international source or market. The future of California agriculture requires action
to conserve biological diversity on a global scale.
California is not the focus of this discussion (though if it were a nation,
the state's agricultural production of over 250 different crop and livestock
commodities would rank it seventh among the nations of the world) but is
noted here to stress the growing international interdependence of agriculture
and biological conservation.
GENETIC CONCERNS
Sustaining agricultural, forest, and aquatic species and their derivatives
will require the continued application of traditional methods as well as rapid
deployment of new biotechnologies based on molecular genetics. Before
noting the extraordinary promise of new genetic engineering technologies,
it is important to look at the potential of conventional plant and animal
breeding methods.
At least half of the increases in productivity realized this century are
directly attributable to artificial selection, recombination, and intraspecific
gene transfer procedures. In addition, interspecific and intergeneric gene
transfer have been practiced routinely for a few cultivated crop species for
50 years and promise to continue contributing to crop improvement as long
as the wild relatives of crop species are conserved.
The success of these traditional plant and animal breeding approaches
notwithstanding, it is important to note that very few of the species utilized
by humans have received intensive scientific attention. Researchers have
focused most of their energy on a handful of grasses (rice, wheat, maize,
and oats), nightshades (tomato, potato, and tobacco), mammals (cattle,
sheep, and pigs), and birds (chickens and ducks), the species responsible for
upwards of 90% of human sustenance.
Molecular genetics and genetic engineering have much to offer to. the
improvement of agricultural species in ways that will both reduce negative
environmental impacts and enhance sustainable productivity.
Major
57
technological progress has been made already in plant genetic manipulation,
industrial tissue culture, genetically engineered animal products, and the use
of genetically engineered microorganisms, to produce agricultural and
medical products.
.'
There are a number of things genetic engineering cannot do, which
should be noted. It is not, for example, a substitute for traditional breeding
methods for the improvement of traits under the control of multiple genes
scattered throughout the chromosomes. Applications of genetically engineered transforms must be supported by traditional genetic testing and field
evaluation procedures.
Most important, genetic engineering and other
biotechnologies cannot be used as a substitute for traditional approaches to
conserving genetic variation. Gene banks and the conservation of wild
relatives provide the raw material for genetic engineering as well as
traditional animal and plant improvements.
Genetic engineering involves altering the genome of an organism by
adding new genes or changing existing genes. Gene transfer, gene recombination, gene expression, and protein synthesis all can be manipulated by
relatively simple in vitro techniques. Current projects involving the planned
release of genetically engineered organisms include: the development of leaf
colonizing bacteria, Pseudomonas fluorescens, genetically engineered to
express a toxin from a second bacterium (Bacillus thun'ngiensis) that protects
treated plants from caterpillars; the development of P. syringae strains that
lacked the ice-nucleating protein gene to protect treated plants from frost
damage; the development of bio-toxin expressing soil-colonizingP. fluorescens
to counter root cutworms; the incorporation of extra sets of growth hormone
producing genes into farmed fish to enhance growth rate and efficiency; and
the development of Rhizobium meliloti with improved nitrogen fixation
properties. Many of the projects involve the release of microorganisms into
the environment and in this respect they differ significantly from the
confined use of genetically engineered E. coli, yeast, mammalian and insect
cells, to produce proteins of medical value like insulin, growth hormone, and
hepatitis antigens.
At a higher level of biological complexity, projects involving the use of
genetically engineered plants are fairly numerous. Successful experiments
have included tobacco plants altered to be resistant to crown gall, caterpillars, and various forms of herbicides, and tomato plants altered to resist a
virus, caterpillars, and an herbicide. In the near future, Success can be
anticipated with other crop plants and with projects aimed at enhancing such
traits as flavor and drought resistance.
These projects all began with the in vitro propagation of plant cells and
tissues, and currently genetically altered plants are typically clones. This
58
places them at the same risk as many cultivars developed by traditional
techniques. In the future, scientists may be able to exploit the somaclonal
variation in cell cultures to increase the genetic diversity of crop plants, but
the feasibility of this approach has yet to be established. Broadening the
basis for genetic diversity will reduce risk as well as allow for' the continued
application of traditional crop improvement. In any event, it is clear that the
existing genetic diversity not incorporated into commercial cultivars must be
kept in reserve for possible future use.
The prospect of transferring genes for nitrogen fixation from rhizobia or
other competent bacteria to crop plants (such as cereals) or of engineering
crop plants to form symbiotic root nodules with rhizobia, promises to be one
of the most important advances in all of agriculture. Despite very rapid
advances in biotechnology, the molecular machinery required for nitrogen
fixation is so complicated that these goals are unlikely to be achieved in the
next decade. At least 17 genes are directly involved with nitrogen fixation;
at least 10 genes are required for nodulation of rhizobia; and, at least 35
genes specific to nodules have been identified in host plants such as
soybeans. Genetic engineering at this level of complexity has never been
attempted. Regardless of these practical difficulties, it can be anticipated that
the approach will some day reduce dependence on nitrogen fertilizers and
their associated costs.
Because of real and perceived risks associated with deliberate or
accidental release of organisms with recombinant DNA, it is important to
reiterate three conclusions of the 1987 National Academy of Sciences (NAS)
report: (1) there is no evidence of unique hazards in the use of recombinant
DNA techniques or in the movement of genes between unrelated organisms;
(2) the risks associated with the introduction of recombinant DNA organisms
are the same as those associated with the introduction of unmodified
organisms; and (3) assessment of the risks of introducing organisms into the
environment should be based on the nature of the organism and the
environment into which it is to be introduced, not on the method by which
the organism was produced.
These conclusions may be oversimplified and dangerously misleading.
In fact, the body of the NAS report, and the discussion by members of the
Ecological Society of America (Tiedje et aI., 1989), stress the need for
careful case-by-case evaluation of the potential ecological consequences of
releasing transgenic organisms into the environment.
Tiedje et al. (1989) and others have begun to outline the types of genetic,
phenotypic, and environmental criteria that must be considered in ecological
risk assessment and the scaling of regulatory oversight. The following
examples, discussed by Tiedje et aI., are illustrative of the types of hazardous
59
outcomes to be avoided: salt tolerant rice might become a major weed in
estuaries, resulting in rice becoming a pest; viral pesticides based on viruses
with broadened host range could infect beneficial species and thus harm nontarget species; the introduction of a highly competitive nitrogen fixing
bacterium, Bradyrhizobium serogroup 123, into agricultural fields has made it
difficult to introduce more effective rhizobia, an example of a disruptive
effect on a biotic community; and, an example of potential conflict of the use
of genetic resources, Bacillus thuringiensis toxin genes have been inserted into
several crop plants and trees to protect them from insects which should
promote the evolution of insect resistance to these toxins - an event with
potentially far reaching, irreversible consequences.
It is clear that the major difference between past and future methods for
the production of improved agricultural products is the speed at which
genetic modifications will be possible in the future. However, as has been
the case in the past, with careful design of new organisms and proper handling and regulatory oversight of environmental releases, many introductions
can be attempted with minimal ecological risk. Nevertheless, agriculturists,
ecologists, and conservation biologists must work energetically and cooperatively to assure society will benefit from these exceedingly complex scientific
efforts. Temporarily, at least, it may be well to remember Daniel Janzen's
(1986) warning:
If nuclear winter threatens all of us and all those things we work to
save, then the nucleotide summer is surely on the other side of the coin.
Yes, genetic engineering can undoubtedly produce all kinds of fantastically useful organisms. But if you are worriedabout what the rabbit did
in Australia, how the sea lamprey clobbered Lake Michigan, or how
European diseases exterminated the original human occupants of the
New World, 'you ain't seen nothin' yet." The metazoans and microbes
that humanity is gearing up to produce are without doubt the largest
threat of all to nature as we know it.
Although the timely development of environmentally safe products
through the use of advanced biotechnologies must be supported, these
developments should occur within the context of a scientifically-based
regulatory policy that encourages innovation without compromising sound
environmental management.
Another set of biotechnologies of importance to agriculture involve
gamete and embryo storage and transfer (see, for example, Smith et al.,
1986).
Various technologies for the collection, storage, evaluation,
quarantine, and utilization of germplasm are under active development.
60
Cryogenic storage of animal cells, gametes, and embryos is a most promising
technique, but has yet to be developed for more than a handful of species.
Frozen cattle semen has permitted the rapid movement of improved
genotypes on a worldwide basis, and embryo transfer promises to augment
this process. In addition, rapid progress is being made in ill vitro fertilization, nuclear transplantation to permit embryo cloning, and semen sexing for
a few domestic animals. These techniques collectively could transform
current animal breeding practices and greatly increase the speed with which
existing populations are adapting to the changing demands of commercial
production. In addition, the potential applications of these techniques to ex
situ conservation, particularly at zoological gardens, have only begun to be
identified and developed.
.
Interspecific gene transfer, using molecular genetic methods, has been
successful in laboratory trials; its potential to modify animal populations in
useful ways has so far not been realized, but could be great. Techniques of
genetic engineering are also playing an important role in increasing animal
productivity by improving vaccines and pharmaceuticals. Examples of the
latter include growth promoting and fertility hormones and proteins of
importance to an animal's immunological state. Hybridoma technology,
which results in the generation of monoclonal antibodies by cell fusion
procedures, will be increasingly useful in diagnosing specific diseases as well
as in disease prevention and treatment.
Certain cryogenic technologies that have promise in conserving plant
germplasm at less than the cost of conventional seed storage are being
developed and used by a number of national and international organizations.
Here, too, standard operating procedures need to be developed for the
collection, sampling, storage, and evaluation of such resources, especially for
non-crop species. If the long-term (100 year) viability of frozen germplasm
can be demonstrated, then these techniques will playa major role in future
genetic conservation.
Finally, the enormous potential contribution of genetics and biotechnology to processes involving fermentation must be noted. Important agricultural
products include proteins for nutritional supplementation, antibiotics used
in health care, and rennins for cheese production. An enormously important
challenge for the immediate future is the application of fermentation
techniques to the conversion of waste byproducts of animal, crop, and food
production to useful end products.
Molecular genetics and associated biotechnologies have a great deal to
offer for the improvement of agricultural species and enhancing conservation
efforts. Combined with improvement in applied evolutionary biology, a
reduction in negative environmental impacts and enhanced resource use and
1.1.8
61
conservation can be anticipated. However, genetic approaches to improving
agricultural systems and conservation programs are deficient in at least three
fundamental ways. First, the genetics of adaptive responses of natural
populations to ongoing climatic, radiation, and pollutant level changes are
poorly understood. Second, the marvels of genetic engineering and
germplasm storage and manipulation are still restricted to an extremely
limited subset of the biological diversity urgently requiring conservation.
Third, far more attention must be paid to genetic aspects of colonists and
weeds and to host-parasite and predator-prey coevolution, so that natural
processes can be better incorporated into future agricultural management
practices.
PATTERNS OF GENETIC VARIATION
In order to evaluate and adequately manage genetic resources, and to
ensure their conservation, it is essential to document patterns of genetic
variation, provide an understanding of the ecological and life-history
determinants that influence these patterns, and assess the importance of
random genetic drift and selection. To date, information of this sort is
available for only a limited number of agriculturally important species and
for a tiny fraction of rare and threatened species (Woodruff, 1989). Indeed,
in the foreseeable future, it is all but certain that only a small proportion of
the 5,000-10,000 plant species of economic value or the 25,000-30,000
threatened plant species will be evaluated in this way.
With current technology, it is impossible to evaluate the genetic variation
and population structure of all species requiring management. Ways must
be developed to prioritize species for attention. For example, with plants it
has been found that genetic variation generally increases as life forms
progress from shorter to longer-lived species (annual plants - herbaceous
perennials; woody perennials - trees). A multidimensional matrix for
classifying population structure within life forms can be defined according to
distribution (widespread vs. restricted, continuous vs. fragmented), density
(common vs. rare), mating system (selfing vs. outcrossing), and pollen
vectors. Representatives of each type can be studied to discover trends and
generalizations. Thus, species with wide geographic ranges, long generation
times, and a wind-pollinated outcrossing mating system (e.g. conifers) tend
to have high levels of genetic variation, mostly within populations. In
contrast, annual herbaceous species, primarily selfing, have lower levels of
variation, mostly between populations.
62
It seems plausible that broad genetic management strategies could be
formulated for biological groups by studying selected indicator species from
a large group of species with similar attributes. By investigating patterns of
genetic variability in both geographically restricted and widespread species
of Eucalyptus, scientists have been able to develop preliminary strategies for
the conservation of genetic resources in other groups of eucalypts with
different geographic population structures. Because the area occupied by a
viable breeding population of a tree species is much larger than the majority
of understory species, the conservation of the former species will more than
likely lead to the protection of a large number of other species.
Genetic marker studies often enable specific decisions to be made
concerning priority populations for conservation and how many populations
are required for adequate genetic resource management. Genetic markers
can be used to identify unique and representative populations, and locally
distributed but common alleles for conservation. As a corollary, it is
desirable also to investigate whether locally common alleles are indicators of
adaptation. Until genetic-environment relationships are better understood,
it will be impossible to distinguish between natural selection and genetic drift
in relation to establishment and maintenance of genetic diversity in local
populations. Although genetic marker studies, particularly those using
allozymes, have greatly increased our understanding, it has not been possible
to describe all the genetic variation in important populations and species.
Measuring genetic variation
Various methods are now available for estimating the amount of genetic
variation present in a population or species. DNA sequences and restriction
fragment length polymorphism (RFLP) patterns can provide direct and
genetically interpretable measures of individual and population level
variation. Data on protein variation using primarily variable enzyme forms
called allozymes, are by far the most common and easily obtained. Estimates
of the average proportion of loci in a population that are polymorphic (P)
and of loci in an individual that are heterozygous (H) are now available for
a few thousand species of plants and other animals.
Generally, most organisms have high levels of variation; for many
outcrossing plants P is greater than 0.4 and H is greater than 0.15. Most vertebrates are slightly less variable than plants; most invertebrates show even
higher levels of innate variability (Nevo et aI., 1984). There are exceptions,
of course, but usually natural populations of plants and animals are highly
63
variable genetically, while smaller, fragmented; inbred, and domesticated
populations are less variable.
Before reviewing the patterns of genetic variation in natural populations
and their exploited derivatives, it is important to recognize the limitations of
the allozymic data base. The question is: to what extent can surveys of
variation for 20-30 soluble proteins, the products of structural genes, be
representative of the genome as a whole? Present indications, based on
surveys of more than 100 allozymic loci in a few species, are that such
surveys may reasonably reflect relative levels of whole genome variation.
This conclusion is supported by emerging data on restriction fragment length
polymorphisms and DNA sequence variation.
Similarly, controlled breeding experiments and artificial selection
generally reveal positive relationships between allozymic and quantitative
variation. The latter is especially important to agriculture because such
genetic systems control many morphological and life history traits. Thus,
despite reservations about the interpretation of allozymic variation, it
presently has advantages of speed and low cost over other methods of
estimating relative levels of genetic variation in populations.
Most allozymic variation is currently regarded as selectively neutral. If
patterns of variation are unrelated to fitness, then recommendations for
germplasm storage, for example, based on a specific set of allozymes mayor
may not be reliable. The case involving the differential fitness of two lactate
dehydrogenase allozymes in mussels living along a thermal gradient is the
most notable exception (Koehn and Hiblish, 1987). There are hints that
relative levels of multilocus allozyrnic variability are positively related to
agriculturally important traits. Genetically variable individuals grow faster
and larger in pines and oysters. Genetically invariant populations are more
susceptible to attack by fungal and viral diseases in maize and some
mammals. Thus, although allozyme surveys are most instructive as to
relative levels of variation, these data do not indicate relative adaptive values
as part of management recommendations for genetic conservation.
The potential contribution of new molecular genetic techniques to the
identification and quantification of genetic variability is still not clear.
However, the field is developing rapidly, primarily with tools for the study
of evolution. A challenge for those working to adapt genetic engineering
technology to the improvement of agricultural production is to assist the
conservation biologist in transferring the technology to studies of population
and species genetic variation. In addition, the increased understanding of
the animal and plant genome resulting from molecular genetic studies will
be invaluable to the conservation biologist in efforts to design efficient
sampling strategies for natural populations.
An integrated agriculture,
64
conservation biology approach will be essential to long-term, broad-based
successes.
Geographical patterns of genetic variation
Patterns of geographical variation can be investigated in two ways. The
first is to demonstrate how different populations show a geographic pattern
in genetic diversity as it may be related to geographical distance, geographically distinct regions, or with peripheral versus central areas of a species
distribution.
The second way is to investigate associations between
geographically varying environmental parameters and genetic variation or
specific gene loci.
With regard to a relationship between geographic distance and genetic
diversity, most recent studies have shown a significant positive correlation
between geographic and multilocus genetic distance, a measure of genetic
differences between populations. These studies have included naturally
distributed populations of various species of pines, eucalypts, game animals,
fish, and shellfish. Typically, specific genetic markers show similar frequencies over wide areas or some gradual geographic clustering. In some cases,
widely distributed species may show marked regional differentiation.
For
instance, four genetically distinct populations of Camelia japonica occur in
different regions of Japan. In other species (e.g. water hyacinths Eichomia
paniculatas, populations differ not only in allele frequencies, but also in
overall levels of variation and other aspects of genetic architecture.
Generally, geographic patterns of allozyme variation are concordant with
current taxonomic practice; i.e. genetically well-differentiated populations are
recognized as distinct races or subspecies. Conversely, genetically similar
populations are treated as belonging to the same species even if they occupy
geographically disjunct areas and do not interbreed naturally. In maize
(corn), races described originally on the basis of ear and kernel characteristics, were, in most cases, identifiable by allozyme analysis. In studies of a
few species, there have been discrepancies between allozymic patterns and
traditional taxonomy that have led to nomenclatural revisions. Well-known,
economically important "species" of mosquitos and frogs turned out to be
groups of closely related cryptic or sibling species. More than two dozen
"species" of economically important freshwater clams were found to be genetically identical and referable to a single biological species.
Comparisons of levels of genetic variation between geographically
peripheral populations and geographically central populations have provided
interesting but ambiguous results. Studies to date indicate that peripheral
65
populations can be either less heterozygous, equally heterozygous, or more
heterozygous than populations occupying the center of the species range.
This result is perhaps not surprising given the importance in distinguishing
that which is ecologically marginal from that which is simply geographically
peripheral. Hence, it is still unclear to what extent a population's ability to
adapt to ongoing environmental changes will be determined by its genetic
variability and architecture.
In many instances, geographical patterns of genetic variation can be
readily interpreted in terms of historical events. It has been proposed, from
the study of a number of North American species, that glaciation resulted in
fragmentation of a species range into small isolated refugia with stochastic
processes (genetic drift) altering allele frequencies among populations and
reducing genetic variability within populations. In some cases, postglacial
changes in distribution permitted genetic exchange (gene flow) between the
genetically differentiated populations; in other cases glaciation may have
resulted in permanently disjunct populations. History also may account for
why, for many North American species, northern populations are less
genetically variable than southern popula tions from which they were presumably derived. Finally, there are cases, with both plants and animals, of the
occurrence of unexpected alleles in some populations; alleles which owe their
presence to previous episodes of hybridization with other species and are
maintained in today's populations as genetic phantoms of unknown
significance.
The presence of correlations between allozyrne frequency and some
environmental parameters across populations of some species has led to the
proposal that geographic patterns of genetic variation can be caused by
selection favoring different genotypes in different environments. There are
a number of studies where associations with environmental variables have
been investigated but in the majority, the question of whether selection is
operating to produce and maintain positive correlations remains unclear.
Most of the plant species studied to date are highly autogamous and, as such,
linkage disequilibrium will decay very slowly and an allozyme locus may
hitchhike with any other locus in the genome. Thus, correlations with
environmental parameters may persist for many generations whatever their
origin.
In a recent study on the outcrossing species Gaillardia pulchella
(blanket-flower), researchers found a significant correlation between certain
allelic variants and edaphic ecotypes indicating the presence of races
adaptively differentiated due to differences in soil type. The researchers
point out, however, that such correlations are not necessarily sufficient to
conclude that the allozyme differences observed between ecotypes are
233
66
mediated by selection. Alternatively, they suggest that if the founding of a
soil ecotype was a unique event, and interracial gene exchange is both recent
and restricted, then allozyme frequency differences could persist because of
the effects of genetic drift. Again, allozymes often tell us a lot about history,
little about adaptation.
Life history characteristics
Life history traits are under complex polygenic control and there is no
a priori expectation that allozymic variation is causally related to their
regulation or expression. This applies to both single locus and multilocus
associations. However, associations between genetic variation and traits of
great importance to agriculture have been the subject of several recent
reviews (Ledig, 1986; O'Brien and Evermann, 1988).
Correlations, even when statistically significant, may be biologically
spurious. Therefore, in this section, the genetic basis of life history traits is
reviewed. However, it is important to begin with a brief look at the
population genetic underpinnings of a number of traits by considering a few
examples.
Individual growth rate. There is a considerable amount of additive
genetic variance for growth in outbreeding species. Multilocus hybrid
superiority is evident in a range of different organisms.
Age of maturity. Much additive genetic variation exists in plant species.
For animals, the situation is less clear but some evidence is available
supporting response to selection and a genetic correlation with growth.
Life span. Domestication has produced many annual derivatives from
perennial plant species, and more recently, perennial crop varieties have
been developed by breeders. The genetic architecture
of the
annual/perennial difference is not well understood. In animals, life span
typically has a high heritability while the heritability of longevity of
production is low.
Fecundity. Considerable genetic variation in progeny per female exists
in both plants and animals. With animals, attention will always need to be
focused on egg quality, and in the case of mammals, on parental care.
Phenology.
Phases of growth and flowering of plants generally show
considerable additive variation exploitable by selection.
Breeding system. Many plant species have evolved a repertoire of mating
systems from asexual systems, such as apomixis, to sexual systems, ranging
from selfing to outcrossing. Animal species are generally less variable, less
67
flexible, and employ genetically-based, eco-behavioral mechanisms to
minimize inbreeding.
Sex ratio. The mechanisms of sex-determination and the regulation of
sex-ratios are affected by both genetic and environmental factors in plants
and animals.
Dispersal: Variation in morphological traits that influence dispersability
is well known in domesticated and wild plant species, but there is little
information on genetic variability. For animals, which exhibit considerable
variability in migratory behavior, little is known about its genetic architecture.
Dispersion. There are many examples in behavioral ecology of variation
relevant to successful management of populations of animal species.
Unfortunately, almost nothing is known about the genetic basis of such
variation. In some plant species, allelopathic interactions affect dispersion
through differential activity on different genotypes.
Of course the critical question is, how do life history traits, which affect
mode of reproduction, mating system, gamete dispersal biology, effective
population size, population spatial structure and geographic distribution,
influence the level and partitioning of genetic variation within and among
populations. A number of major reviews have demonstrated that allozyme
variation within species is associated to a greater or lesser extent with these
factors and that their level of influence differs among different taxonomic
groups. On the other hand, animal and plant breeders have demonstrated
repeatedly that life history traits are all amenable to genetic modification,
through selection, cross breeding, or both. Thus, the question arises as to
whether life history traits of natural populations control the distribution of
genetic variation or whether they are a genetic response to the environmental niche chosen by the species.
There is no doubt that one of the most influential factors in the
organization of genetic variation is the breeding system. Selfing species tend
to show less variation but variation is maintained by a significant proportion
of the variation being partitioned among, rather than within, populations.
As predicted, species that reproduce primarily by outcrossing show the
opposite trend, with much of their genetic variation occurring within populations with little differentiation occurring between populations.
The
importance of utilizing this information in genetic conservation strategies is
clear; more populations of a selfing species are required to conserve similar
levels of genetic variability than is the case with outcrossing species.
Geographic range has not generally been considered an accurate
predictor of patterns of genetic variability.
Some species with small
geographic ranges exhibit significantly lower levels of genetic variation than
2.35
68
their widespread congeners, while others are found to be as variable as their
widespread congeners. These diverse results reflect the complicating effects
of historical factors and habitat heterogeneity, as well as the more fundamental problem of having no reason to expect allozymic variation to be a
determinant of a species geographic distribution.
GENETICS OF !NVASIVE SPECIES
Much of the success of modern agriculture is a result of the cultivation
of various plants and animals often distant from their geographic place of
origin. Classic examples of successfully introduced species include Chinese
soybeans in the United States, European sheep in Australia, and Andean
potatoes in Europe. The deliberate movement of such species by humans
is analogous to the natural processes of dispersal and successful colonization.
Pest species and weeds also fall into the category of successful invaders.
It is not surprising, therefore, that scientists have been especially interested
in the genetic aspects of successful colonization. An understanding of the
genetic constraints on invasibility would make it easier to establish desirable
species in new areas and, conversely, perhaps retard the spread of undesirable species.
The urgent need to improve our understanding of the ecological and
genetic aspects of colonization is underscored by the fact that most attempts
to translocate arthropods for biological control purposes fail. An improved
understanding of colonization is also a requirement if species which require
reintroduction in the wild are to be adequately managed for the conservation
of natural communities.
From studies to date it is clear that there is no unique suite of characteristics found in plant or arthropod species which successfully invade or
colonize new areas (Parsons, 1983; Mooney and Drake, 1986; Drake et al.,
1990). Successful colonists can be found among organisms of widely
divergent genetic constitutions. For example, only a small number of species
appear to be preadapted to the rapid colonization of disturbed habitats.
Perhaps they possess a limited but suitable range of appropriate genotypes.
Conversely, it seems that the successful colonization of intact communities
may require a broader base of genetic variability and a gradual process of
invasion involving local adaptation based on selection and recombination.
The range of genetic attributes of successful invaders indicates that there
is no single optimal solution to the colonization of a new environment.
Although it. may be advantageous for a colonizing populatlon to have
relatively high levels of genetic variation, a number of invasive species have
69
been shown to be genetically uniform. A significant number of surveys of
allozyme variation in weed species document depauperate amounts of
genetic variation both within and between populations, particularly following
continental migration. These findings indicate that high levels of allozyme
diversity are not a prerequisite for a successful colonization. Conversely,
studies on other invasive plant species have revealed remarkably high levels
of genetic variability following colonization.
Assessing the importance of genetic variation during successful
colonization is further complicated because adaptation to varying environments not only involves genetic variation but also phenotypic plasticity.
Phenotypic plasticity probably plays an important role in enabling populations to survive and reproduce in unpredictable environments. At present,
we know little about the relationship between phenotypic plasticity, fitness
of individuals, and underlying genetic variation.
Since colonizing new areas is often initially associated with periods of low
population density, it seems likely that outbreeding species would be less
successful than self-fertilizing or asexually reproducing species. This is
reflected in studies which indicate that selfing or apomixis are significantly
more common in colonizing or invasive plant species than is outbreeding.
However, both obligate outbreeding and vegetative propagation are
frequently associated in perennial weeds.
Another factor proven to be important in the success of weedy plant
species is polyploidy. The 18 most widespread and successful weeds are
believed to be of polyploid origin. This is perhaps not unexpected when one
considers that polyploids potentially have wider adaptability with fixed
heterozygosity reducing the effects of inbreeding and gene duplication
enabling wider environmental tolerance.
One of the major difficulties in the study of invasive species is the lack
of information on the critical very early stages of colonization. This lack
reflects an inability to predict the success of a colonizing event and the need
for comparative studies on related species groups containing both invasive
and non-invasive species.
Disease and pest control
Population vulnerability is probably the most important reason for such
a worldwide interest in genetic variation of domesticated species. The
relationship between low levels of genetic variation and susceptibility to
disease in animals is reviewed by O'Brien and Evermann (1988). The
narrow genetic base of most major crop plants, as documented by the
70
distribution of rather few genotypes per variety, is a major cause of disease
and pest epidemics and their resulting boom-and-bust cycles of agricultural
yields. A wider genetic base (use of either larger number of tested cultivars
per region or heterogeneous populations derived from mixtures or composite
crosses of varieties) is highly recommended and is being investigated in
several crops. A deeper understanding of genetic variation is clearly
essential for the future enhancement of disease or pest resistance.
The use of major genes for race-specific (vertical) resistance which tends
to fail against an evolving pathogen with new virulent races, needs to be
compared with the use of so-called nonspecific or horizontal resistance.
Information about the spatial distribution of genetic variation within
pathogen populations is extremely limited.
Although animal-parasite models generally incorporate both genetic and
ecological parameters, the theoretical models of plant-pathogen interactions
have been dominated by genetic considerations. Ecological factors,like host
and parasite/pathogen patchiness, need to be integrated with detailed studies
of the distribution of infectivity, susceptibility, and virulence genes.
With respect to pest control, the move from dependence on chemical
methods is well underway in California - hastened by the adoption of
appropriately tough anti-pollution laws. Future control methods will rely
more on the integration of genetic and ecological techniques.
Future
practices also will involve careful reconsideration of what constitutes a pest
or a weed. For example, certain weeds are important and useful elements
in agricultural land use systems, of value in erosion control, conservation of
soil moisture, nutrient cycling, and the preservation and enhancement of
natural enemies of crop pests. Future livestock and plant protection will have
to be based more on the genetic and ecological underpinnings that have
sustained natural biological diversity.
PHENOTYPIC PLASTICITY AND SPECIES·LEVEL CONSERVATION
The above discussions have followed convention and emphasized the
importance of allelic genetic diversity. It must be recognized, however, that
phenotypic plasticity deserves far more formal attention as a factor
controlling the future of numerous species. Phenotypic plasticity is the
ability of a single genotype to produce alternative forms of morphology,
physiology and/or behavior in response to environmental conditions. Such
variation, unimodal or discretely bi- or polymodal, is controlled by conditionsensitive switches, allelic switches, or a combination of genetic and environmental factors.
71
Phenotypic plasticity is very important in the evolution of numerous
species and traits of agricultural interest. Familiar examples of alternate
phenotypes produced by such plasticity include: the different vegetative
forms of Brassica oleracia (cabbage, cauliflower, Brussels sprouts, kale,
broccoli, kohlrabi); carrot subspecies and varietal color classes; discrete seed
size classes in four species of Phaseolus beans; the different castes of social
insects including honeybees; and the solitary and swarming phases of locusts.
Such plastic variation is important because natural and artificial selection can
initiate and amplify differences within and between populations rapidly.
Relatively simple changes in one trait can have a cascade of correlated
effects. The origin of corn, Zea mays, from a teosinate might be accounted
for, for example, by a simple change in branch internode length bringing
male tassels into the zone of feminizing hormones, automatically producing
plants with several distinctive morphological traits typical of modern corn.
The role such phenotypic plasticity has played in the evolution of
agricultural species can no longer be ignored. In a rush to account for all
phenomena in terms of genes, the extremely important role of the environment in shaping phenotypic expression may have been ignored. Rather than
being an embarrassment, environmental effects in genetic experiments and
field trials are extremely useful in dissecting the true genetic regulation of
phenotypic traits of interest. As the genetic basis of phenotypic plasticity
becomes better understood, it is important that managers devote more effort
to conserving this very important aspect of overall genetic diversity. For
recent technical reviews of the importance of genotype by environment
interactions in evolution generally, the reader is referred to Schlichting
(1986) and West-Eberhard (1989).
Biological diversity and community conservation
Finally, genetics can be applied at levels of organizational complexity
above those of the individual, population, or species. Some of the issues
have already been alluded to, such as the genetic correlates of the fragmentation of geographic ranges of ecologically key species which can have
profound effects on associated species. This is especially important to
managers concerned with pollinators, parasite vectors, and intermediate
hosts and obligate symbionts. Similarly, attention has been drawn to the
need to develop a robust predictive science of invasibility in terms of the
success of colonists, introductions, and reintroductions. This final section
considers two other important issues: tropical communities and the genetic
basis of higher productivity under mixed farming systems.
72
Interest in the processes that may promote biological diversity has
increased in the last few years as more scientists have become concerned
about the great species diversity in the tropical rainforests. Of relevance is
whether patterns of genetic diversity are in any way associated with patterns
of biological diversity. These associations can be investigated, at least in a
broad sense, by comparing patterns of allozyme diversity in plant species
from diverse areas such as the tropics, with those for species from less
diverse temperate regions. Unfortunately, at present there are few allozyme
studies on tropical plant species and those which have been carried out are
inconclusive with regard to patterns of genetic diversity in tropical versus
temperate regions. Although many tropical tree species contain levels of
allozyme variation equal to or greater than those found in temperate tree
species, there are exceptions.
Whether biological diversity should significantly influence patterns of
genetic diversity is perhaps open to debate given the importance of other
factors such as mating system, life cycle, and population structure. Yet there
is experimental evidence to suggest that in some instances species diversity
may indeed have an effect on genetic diversity. Recent studies have indicated
that genotypic fitness is sensitive to both the presence and identity of
neighboring plant species. Not only do different species constitute different
environments but different genotypes of neighboring species also constitute
different environments; the genotypic performance of one species is sensitive
to the genetic structure of competing species. If this is the case, then it
seems feasible that greater species diversity, such as occurs in the tropics,
could result in generally higher levels of genetic diversity necessary for
adaptation to the many micro environments represented by the numerous
competing neighboring species.
Finally, with respect to mixed farming systems of polyculture and
intercropping, the genetic aspects of new "ways" of farming are only just
beginning to receive scientific scrutiny (Vandermeer, 1989). Intercropping
refers to some well-known cropping systems such as corn-bean, wheatmustard, amaranth-millet mixes, to which plant breeders can make contributions through designing plant architecture to fit optimal plant density, sowing,
and harvesting practices. Genetic resources in each of these crops are now
being utilized for such breeding work. Similar ideas are proposed for
aquaculture and horticulture. As an example of the latter type, many fruit
orchard owners also grow cover crops.
Likewise, "mosaic" farming, under which plots of several different crop
species are interspersed, requires plant breeding research aimed toward
better pest and disease control. Certain pest species are differentially
attracted to one of these species such that it protects the other species. Many
73
cropping systems, developed prior to the modern high-input monoculture,
provide excellent examples of species mixtures and multiple resources. Such
complex agricultural communities will become increasingly important as
society moves towards sustainable agriculture.
REFERENCES
Drake, J.A., de Castri, F., Groves, R, Kruger, F., Mooney, H.A., Rejmanek, M. and Williamson, M.W.
(Editors), 1990. Biological Invasions: A Global Perspective. John Wiley, Winchester, England.
Janzen, D.H., 1986. The eternal external threat. In: M.E. Soule (Editor), Conservatlon Biology. Sinauer
Assoc., Sunderland, MA, pp. 286-303.
Koehn, RK and Hilbish, TJ., 1987. The adaptive importance of genetic variation. Amer. Sci., 75: 134.141.
Lande, R, 1988. Genetics and demography in biological conservation.
Science, 241: 1455.1460.
Ledig, F.T., 1986. Heterozygosity, heterosis, and fitness in outbreeding plants. In: M.E. Soule (Editor),
Conservarlon Biology. Sinauer Assoc., Sunderland, MA, pp. 77.104.
McNeely, J.A., Miller, KR, Reid, W.V., Mittermeier, R.A. and Werner, T.B., 1990. Conserving the
World's Biological Diversity. IUCN, Gland, Switzerland; WRI, CI, WWF·US, and the World Bank,
Washington, De.
Mooney, H.A. lind Drake, J.A. (Editors), 1986. Ecology of Biological Invasions of North America and
Hawaii. Springer-Verlag, NY.
National Academy of Sciences, 1987. Introduction of recombinant DNA-engineered organisms into the
environment: Key issues. National Academy Press, Washington, DC.
Nevo, E., Beilles, A. and Ben-Shlomo, R, 1984. The evolutionary significance of genetic diversity:
Ecological, demographic and life history correlates. In: G.S. Mani (Editor), EVOlutionary Dynamics
of Genetic Diversity. Springer-Verlag, ~'Y, pp. 13-213.
O'Brien, SJ. and Evermann, J.F •• 1988. Interactive influence of infectious disease and genetic diversity in
natural populations. Trends Ecol. Evol., 3: 254.259.
Parsons, P.A., 1983. The EVOlutionary Biology of Colonizing Species. Cambridge University Press, NY.
SchliChting, e.D., 1986. The evolution of phenotypic plasticity in plants. Ann. Rev. Ecol. Syst., 17: 667-693.
Smith, C., King, J.W.B. and McKay, J.C. (Editors), 1986. Exploiting New Technologies in Animal Breeding.
Oxford University Press, London.
Soul.!, MoE. (Editor), 1986. Conservation Biology. Sinauer Assoc., Sunderland, MA.
Tiedje, J.M., Colwell, R.K, Grossman. Y.L., Hodson, RE., Lenski, RE., Mack, RN. and Regal, PJ., 1989.
The planned introduction of genetically engineered organisms: Ecological considerations and
recommendations. Ecology, 70: 298·315.
Vandermeer, J., 1989. The Ecology of Intercropping. Cambridge University Press, ","'Y.
West-Eberhard, MJ., 1989. Phenotypic plasticity and the origins of diversity. Ann. Rev. Ecol. Syst., 20:
249·278.
Wilson, E.O. (Editor), 1988. Biodiversity. National Academy Press, Washington, De.
Woodruff, D.S., 1989. The problems of conserving genes and species. In: D. Western and Moe. Pearl
(Editors). Conservation for the Twenty-First Century. Oxford University Press, 1\1')', pp. 76-88.
Lit'