Genetic Diversity and Its Conservation in Natural Populations of Plants

Genetic Diversity and Its Conservation in Natural Populations of PlantsAuthor(s): Alan GraySource: Biodiversity Letters, Vol. 3, No. 3 (May, 1996), pp. 71-80Published by: WileyStable URL: http://www.jstor.org/stable/2999720 .

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Biodiversity Letters (1996) 3, 71-80

BIODIVERSITY RESEARCH

Genetic diversity and its conservation in natural

populations of plants

ALAN GRAY Institute of Terrestrial Ecology, Furzebrook Research Station, Wareham, Dorset, BH205AS, U.K.

Abstract. This paper reviews patterns of genetic diversity in natural populations of plants: patterns which have emerged from more than 70 years of

genecological investigation and 30 years of allozyme analysis. The compelling conclusion to be drawn from these empirical studies is that genetic diversity in most plant species lies along the axis of environmental, and specifically habitat, variability. This predominance of genotype-environment correlations, a testimony to the power and ubiquity of natural selection, demands that strategies for the conservation of genetic diversity involve sampling or protection schemes which are stratified across environments or habitat-types. The genetic response of species' populations to their environment is affected, or constrained, by a range of intrinsic

biological properties such as the breeding system and external processes such as those which cause fluctuations in population size. Insight into the impact of such forces on the genetic diversity and structure of natural populations has been the major gain from studies of allozyme variation. However, there is some doubt about the neutrality of allozyme loci, and often no correlation can be found between levels of

INTRODUCTION

The aims of this paper are (i) to discuss, and where

appropriate provide some generalizations about, spatial and temporal patterns of genetic diversity in natural populations of plants, and (ii) to consider strategies for its conservation (both in situ and as a basis for sampling for ex situ conservation). These are ambitious aims. They can only be achieved in the space available by adopting a fairly eclectic approach?for which, to those seeking a comprehensive review, I should apologize in advance.

allozyme variation and those in quantitative trait loci. Furthermore, variation in intrinsic properties and external forces accounts for relatively small amounts of the between-species variation in genetic diversity (but rather more of the variation in their

population genetic structure). Coupled with the remarkable, and largely unpredictable, range of

diversity patterns found in rare and endangered species, this has led to the view that there are no useful generalizations on which to base conservation strategies. Each and every species must be

investigated. Here I suggest that this view has been based on an inappropriate group of species (the rare and endangered) and that a habitat-based conservation strategy has generic utility. Because of the remarkably small numbers of plants needed to

capture most of a species' genetic diversity, sampling, or conserving, across habitats can be adjusted to account for the expected levels of between-population diflerentiation. Prediction of these levels may be

improved by taking a phylogenetic approach.

Key words. Genetic diversity, genotype-environment correlations, allozymes, conservation, natural

populations of plants, phylogenetic approach.

PATTERNS OF DIVERSITY

Genotype-environment correlation

Contemporary treatments of the subjects of

biodiversity, genetic diversity and conservation genetics rarely fully acknowledge, and frequently ignore, the contribution of the early plant genecologists. Yet the

pioneering work of Gote Turesson in Sweden in the 1920s and ofthe Carnegie group, notably Jens Clausen, David Keck and William Hiesey, in North America in the 1930s and 1940s, had established more than 50

years ago at least two important general principles: namely that patterns of heritable variation within and

? 1996 Blackwell Science Ltd 71



72 Alan Gray

among populations of plant species are often broadly relatable to environmental variation, and that populations from similar habitats often display similar traits. On a broad geographical scale, a 200-mile transect at 38?N latitude across California, variation in species such as Potentilla glandulosa and Achillea millefolium, as measured by growth in three experimental gardens at contrasting altitudes, could be related to the climate and altitude of the population of origin (Clausen, Keck & Hiesey, 1940). On a habitat scale, populations of Hieracium umbellatum from sand dunes in different regions of south Sweden were shown to be more alike morphologically than populations from dunes, fields and woodland in the same region (hence sand dune ecotypes) (Turesson, 1922).

Turesson, the Carnegie group, and others such as Gregor and his associates in Britain and Sinskaia in the USSR, were greatly concerned with delimiting intraspecific taxonomic categories based on the patterns of variation they observed in common garden experiments. There was much lather about ecotypes versus ecoclines, geographie subspecies and topoclines. But it would be a great mistake to dismiss these early studies as merely descriptive and not concerned with processes. Indeed, their scope and scale richly illustrate the maxim that there is very little completely new under the sun (and the one about reinventing the wheel). Issues such as the respective importance of genetic differentiation and phenotypic plasticity and the

persistence of small-scale differentiation in the face of gene flow, were raised (and discussed, for example by Turesson's work on prostrate maritime populations of Succisa pratensis and Aster tripolium (Turesson, 1925) and by Gregor's work on clinal variation in coastal Plantago maritima (Gregor, 1938, 1946), respectively). Modern preoccupations, such as the measurement of selection pressures by reciprocal transplanting, the analysis of the genetic control of traits and of correlations between traits, and the comparison of reproductive performance and breeding systems in different populations, were all covered in these early studies.

Especially notable was their scale. For example, F. E. Clements and his associates, in a relatively little- known study covering more than 40 years (Clements, Martin & Long, 1950), cultivated over 700 species in five experimental gardens?three in Colorado and two in California. Many thousands of plants were grown for up to five generations, often in a range of soils and

light intensities and including, at the Santa Barbara

garden, length-of-day tents which were moved over the

plots on rails. In a series of competition cultures, 4, 16, 64, 128 or even 256 individuals were grown in standard-sized plots in experiments which foreshadowed the current interest in the effects of plant density. Also included were reciprocal transplants to different altitudes, batteries of recording instruments at a range of climatic stations, and even the use of phytometers (living plants) to measure variation in

transpiration rates. Although E. M. Marsden-Jones and W. B. Turrill, working mainly at Kew in the UK, concentrated on relatively few species, the scale of their experiments was similarly impressive. Research on three species in the genus Centaurea involved measuring more than 24,000 plants, almost half from controlled breeding experiments, and in that on two species of Silene around 130 natural populations were sampled and 368 controlled crossings and selfings made (Marsden-Jones & Turrill, 1945). Both studies spanned more than 30 years of comparative cultivation and transplant experiments.

In some ways, a major legacy of this detailed early genecological work (successively reviewed by Heslop- Harrison (1964), Langlet (1971) and Briggs & Walters (1984)) was the impression that analysing genetic variation in natural populations is impossibly difficult. The variation is too complex. There are too many genes and too many interacting factors controlling their transmission and distribution. Certainly, for those

investigators who were seeking elaborate and detailed proof ofthe Darwinian process of evolution by natural selection, as most were, the really interesting traits, i.e. those affecting fitness, appeared to be polygenically controlled and remained elusively beyond the reach of formal genetic analysis. Major genes were few (but see Gottlieb (1984) for a different perspective) and, until the advent of the work by Bradshaw and his colleagues on heavy metal tolerance in grasses (see, e.g. Bradshaw & McNeilly, 1981), seemed to have small effects on fitness. In more recent years, the rush to measure variation in gene products with simple modes of inheritance, notably isozymes, plus the labours involved in estimating quantitative genetic parameters such as narrow-sense heritability (h2) or additive genetic covariance between traits (COVA) with their protean, environment-specific nature, may have reduced interest in population differentiation in so-called fitness or

ecologically-relevant traits. Elegant and famous criticism of the adaptionist approach to evolution (Gould & Lewontin, 1979) is likely to have provided further discouragement.

Despite this, the growing literature is rich in examples

? 1996 Blackwell Science Ltd, Biodiversity Letters, 3, 71-80



Genetic diversity in plants 73

of correlations between genetic variation and environment which could sensibly be interpreted as resulting from what Turesson (1922) called a genotypical response to habitat. Some authors merely hint at the possible causes of such correlations, as though surprised to find them. Others go further and seek experimental evidence, both for modes of inheritance and mechanisms of selection. The variety is astonishing: thus one finds, even in the early classic studies, examples of genetically complex traits with abrupt differentiation patterns, e.g. several life-history characters in the grass Anthoxanthum odoratum in the Park Grass Plots (Davies & Snaydon, 1976), genetically simple traits with puzzlingly complex or clinal distribution patterns, e.g. cyanogenesis in Lotus corniculatus (Keymer & Ellis, 1978) or seed-coat pattern in Spergula arvensis (New, 1978) and both abrupt and gradual differentiation in the same trait in the same species, e.g. stolon length in coastal populations of Agrostis stolonifera (Aston & Bradshaw, 1966). A far- from-systematic survey of the author's reprint collection reveals numerous examples of genetic differentiation within or among natural populations in

apparent response to a wide range of environmental stresses. These include (limiting the examples to two) salinity (Agrostis stolonifera (Kik, 1989), Centaurium littorale (Freijsen & van Dijk, 1975)), fungal pathogens (Glycine canescens (Burden, 1987), Amphicarpaea bracteata (Parker, 1988)), herbivores (Pinus edulis (Mopper et al, 1991), Cenchrus incertus (McKinney & Fowler, 1991)), plant competition/density (Bouteloua rigidiseta (Miller & Fowler, 1994), Plantago lanceolata (Wolff & van Delden, 1987)), variation in altitude

(Capsella bursa-pastoris (Neuffer, 1990), Pinus flexilis (Schuster, Alles & Mitton, 1989)), and latitude (Daucus carota (Lacey, 1988), Campanula americana (Kalisz & Wardle, 1994)). Traits clearly under selection include some relatively new genes, e.g. herbicide-resistance in an increasing number of species (Powles & Holtum, 1994) and some familiar genes, e.g. zinc-tolerance, in new species (e.g. the moss Funaria hygrometrica?Shaw, 1988) or in familiar species in novel environments (in Agrostis capillaris and Dechampsia cespitosa beneath electricity pylons?Al-Hiyaly et al, 1993; Coulaud & McNeilly, 1992).

The conclusion we must draw from this wealth of studies spanning more than 70 years is that most of the genetic diversity in most plant species populations lies along the axis of environmental, and specifically habitat, variability. This completely intuitive, even trivial, generalization is rarely made explicit (but see


later). This may be through fear of adaptionism, or the reductionist need always to fill in all the complex steps between correlation and causation, or even because it implies further defence of the rather weak- sounding natural history-based argument that the optimum species conservation policy is to maintain as many populations in as many different habitat-types as possible across the species' entire geographie range. It is nevertheless a truism which those who seek to sample and exploit the genetic diversity in natural populations?the plant breeders?have known for many years (e.g. Frankel & Bennett, 1970).

Allozymes and marker genes

What, by comparison, have we learned from 30 years of work on allozymes (the first population data for allozymes?albeit in Drosophila and humans?having been published in 1966 by Lewontin & Hubby and Harris, respectively)? I believe that there has been no

major single lesson but, instead, a series of powerful insights into the factors which shape genetic diversity and structure in plant populations (structure is a key word here, much having been learned not only about how much diversity species contain but also how that

diversity is distributed within and among populations). The ease of detection, Mendelian inheritance and codominant expression of variation at most isozyme loci have generated an enormous dataset and the facility to estimate and compare key genetic parameters (such as the proportion of loci that are polymorphic (P), the proportion of heterozygous loci in the average individual (H), overall gene diversity (HT), or various estimates of the partitioning of diversity within and

among populations (FST, GST, etc.)). The factors which shape genetic diversity in plant

populations can roughly be divided into two groups: (i) the intrinsic biological properties ofthe species; such as the genetic (recombination) system including the

breeding system, ploidy level and meiotic behaviour, the mode of pollination and seed dispersal, and the life form (annual, perennial, woody, clonal, etc), and (ii) extrinsic dynamic processes which affect species' populations, such as fluctuations in size including bottlenecks, invasions or founding events, changes caused by ecological succession, and a whole range of historical and contemporary events ranging from Pleistocene glaciation patterns to modern agricultural practices.

These factors combine and interact, of course, to

produce contrasts such as endemic, inbreeding annual



74 Alan Gray

herbs of early successional stages and geographically widespread, outbreeding trees of climax woodland. However, their respective contribution to the patterns of diversity has been dissected in various reviews of the burgeoning plant allozyme literature, principally by J. L. Hamrick and his colleagues (Hamrick, Linhart & Mitton, 1979; Hamrick, 1983; Loveless & Hamrick, 1984; Hamrick & Godt, 1989; Hamrick et al, 1991?see also Brown, 1979; Gottlieb, 1981 and Avise, 1994). Some general trends have emerged.

The intrinsic biological property which appears to have the largest single influence on patterns of allozyme diversity is the breeding system. Self-incompatible species not only have, on average, significantly more individuals heterozygous at polymorphic loci (H) than do selfing species but also significantly higher levels of overall genetic diversity (HT). Of particular interest is the contrast in the partitioning of genetic diversity among populations. In Hamrick & Godt's (1989) analysis of more than 400 taxa, selfing species had more than 50% of their total diversity among populations (GST = 0.51) whereas outcrossed, wind- pollinated species had around 10% (GST = 0.10)?a fivefold difference. In the same survey, annual species had nearly fourfold more diversity among their populations than long-lived, woody perennials, and together breeding system and life form accounted for 84% of the variation in GST among species which could be explained by the traits examined (and almost 40% of the total variation in GST among species). The combination of breeding system and life form may largely account for the sort of extreme contrast in population genetic structure seen, for example, in two grass species with similar distributions in south-west Britain (Gray, 1996a). With one exception, all twenty- two alleles at nine loci were found in every one of the thirty populations of the perennial outbreeder Agrostis curtisii sampled across its range (albeit at different frequencies), whereas in the annual selfing species Gastridium ventricosum, although all the alleles at each locus were present across its range, populations contained only one allele each at five loci and one allele in nine out of eleven populations at a sixth locus (with only one locus containing more than one allele in the majority of populations) (John, 1992). The implications of such contrasting population genetic structure for a conservation strategy are enormous (see below and Gray, 1996a). Other aspects ofthe intrinsic biology of the species which help to explain at least some of the variation in genetic diversity include its taxonomic status (dicot, monocot, gymnosperm) and its seed

dispersal mechanism (explosive, animal dispersed, gravity dispersed) (Hamrick & Godt, 1989).

Such intrinsic biological properties of a species (which incidentally are not fixed but may vary within species over space and time, e.g. the rate of outbreeding) can be seen as determining, or constraining, the response which the populations of that species make to the range of external forces acting on them?forces including habitat perturbation by fire, herbivory or successional changes, or chance long-distance dispersal. Consequently, species whose populations have experienced similar dynamics may display similar genetic structure. This is reflected in the fact that differences in geographic range and successional status appear to explain some of the differences in diversity among species. In Hamrick & Godt's (1989) survey, endemic species had less than half the genetic diversity of geographically-widespread species with a smaller proportion of polymorphic loci and fewer alleles per polymorphic locus (although the partitioning of diversity among populations of endemic and widespread species was very similar). Studies of individual species, or cogeneric pairs, with widespread and restricted distributions have highlighted similar contrasts (e.g. Eichornia paniculata (Glover & Barrett, 1987) and Erythronium propullans and E. albidum (Pleasants & Wendel, 1989) (see also Karron, 1987). The impact on genetic diversity of sudden reductions in population size such as founding events and invasions has been demonstrated many times (e.g. bottlenecks in Sarrancenia purpurea (Taggart, McNally & Sharp, 1990) and Stylidium coroniforme (Coates, 1992), or spread following invasion of new territory by Bromus tectorum (Novack, Mack & Soltis, 1991) or the creation of an allopolyploid, as in Spartina anglica (Gray, Marshall & Raybould, 1991)).

Although general contrasts are drawn between the patterns of genetic diversity found in early and late successional species (Hamrick & Godt, 1989), it is not clear what successional mechanism might be responsible, or indeed whether, lacking a phylogenetic dimension (see below), the comparison is spurious (e.g. early successional species happen to be dominated by phylogenetically similar taxa). Based on studies of succession in populations of the saltmarsh grass Puccinellia maritima and a post-fire population of the heathland grass Agrostis curtisii, plus a review of similar studies, Gray (1987) characterized genetic change during succession as typically a process of genotype or biotype depletion following the initial colonizing phase and often extended over many years.





The work on Puccinellia maritima utilized allozyme variation to analyse the clonal diversity of different populations (Gray, Parsell & Scott, 1979), as did that by Silander (1979) on Spartina patens. As with their use as markers of genetic structure, the employment of allozymes to characterize clonal diversity is being superseded by a range of more sensitive methods which detect variation at the DNA level (e.g. in Populus tremuloides (Rogstad, Nybom & Schaal, 1991)). These molecular markers may not only reveal more variation than is detectable by allozymes (see e.g. Bachmann, 1994) but also add to the growing evidence that allozymes should not as a matter of course be regarded as neutral markers. The evidence comes from general comparisons, e.g. variation at PGI loci in many plants and animals displays correlation with several environmental conditions (Riddoch, 1993), and from

specific cases such as the recent studies on the grasses Bromus hordeaceus (by Lonn, 1993) and Festuca ovina (by Prentice et al, 1995) which indicate that selection, direct or indirect through linkage, is controlling the distribution of allozymes in at least some natural populations. Raybould, Mogg & Clarke's (1996) comparison of RFLPs and isozymes in the same Beta maritima populations suggests that the former neutrally reflect the effects of gene flow whilst the latter fail to fit an isolation-by-distance model, and may be under balancing selection. Finally, we should be aware that variation, or lack of it, in genes controlling allozymes may not match that in other genes (e.g. in Primula scotica (Ennos et al, 1996)) and in such cases may give a misleading picture ofthe amounts and distribution of diversity.

CONSERVATION OF DIVERSITY

Are generalizations possible?

The first question which arises in attempting to seek a generic scheme for conserving wild plant diversity is:

given the complexity of variation patterns and causes outlined above, do any useful general principles exist? Must we treat every species as likely to be different in some way from all those we have already studied? Kay and John (1996) firmly believe we should. Advocating the direct study of each individual species, they dismiss inferences and generalizations from apparently similar situations in other plant species, and even from other

populations of the same species as being often

inapplicable, sometimes dangerously so (Kay & John,


1996). Theoretical modelling, too, they regard as likely to be extremely misleading. In support of these assertions they report the analysis of allozyme variation in more than thirty rare or declining species in Britain and Ireland, emphasizing the remarkable variability and unpredictability of the genetic structures that they find.

Perhaps it is not surprising that this view prevails, since virtually the only common feature of the species studied by Kay & John (1996), and by several others concerned with conserving genetic diversity (Falk & Holsinger, 1991), is that they are rare or declining or comprise small and/or isolated populations. The reasons for their membership of this group are often completely disconnected with the forces, intrinsic or extrinsic, which shape genetic structure. Kay and John themselves list glaciation, Neolithic forest clearance, wetland drainage, and changes in agricultural practice, including the use of herbicides and fertilizers, among the complex of historical factors which have led to an increasing fragmentation and rarity in the British flora (Kay & John, 1996). This suggests that rare or declining species in a disturbed and highly human-influenced environment, are a totally unsuitable group among which to seek generalizations about patterns of genetic diversity. When we remember that the picture of diversity provided by a survey of allozyme variation in a species' populations may be an unreliable guide to the diversity in that species in traits under selection, the situation seems even more hopeless. Perhaps for rare species in exploited landscapes there can be no short cuts. Without the benefit of a survey, we may be forced to say that as many populations as possible ought to be conserved, protected in situ or sampled for ex situ conservation.

Furthermore, the analyses of Hamrick and his colleagues, whilst displaying clear trends, account for relatively small amounts of the total variation in

allozyme diversity. Multiple regression of eight groups of traits accounted for only 24% of the variation at the species level, 28% of the variation in population- level diversity, and 47% of the variation in GST values (Hamrick et al, 1991). Again, however, the dataset of more than 450 species reflects to some extent the

preoccupation of conservation geneticists with rare and endangered species (or special groups of species such as colonizers and invaders).

Despite these problems, I believe there are at least three reasons for being more optimistic about devising a general strategy for conserving genetic diversity. Roughly speaking, these are (1) the pervasive patterns



76 Alan Gray

of genotype-environment correlations in natural populations of plants, (2) the small minimum sample sizes needed to conserve most of the genetic diversity present in such populations, and (3) the enormous potential of a phylogenetic approach where little is known in advance about the diversity.

Strategies for conserving diversity

The first point, that genotype-environment correlations are an almost universal feature of the patterns of

diversity in natural plant populations, was discussed in detail above. The amount of genetic differentiation between populations in different environments will vary from species to species. It will be countered by historic events and random processes such as genetic drift. Nevertheless, the power and ubiquity of selection, and of the response of species' populations to selection, demands that sampling (whether by protection in situ or collection for ex situ conservation) is stratified across environments or habitat-types.

Where the population genetic structure of a particular target species is unknown, the sensible approach to maximizing genetic diversity is to defend populations from as wide a range of environments, geographie and ecological, as possible. Rarely emphasized in modern discussions of genetic conservation, this simple reasoning provided the basis of the earliest published strategies for germplasm collection of crop relatives aimed at optimizing the diversity in the sample (Allard, 1970). These strategies advocated the collection of rather a large number of seeds or plants?Allard suggested a seedhead from 200-300 plants in each of 500 populations for Avena sterilis. The subsequent development of detailed practical sampling strategies has concentrated on ways of reducing the numbers?by biased sampling of variants, fewer populations, and so on (Marshall, 1989). Nevertheless, the principle of habitat-based sampling or conservation remains. For example, in discussing rare British grasses, Gray (1996b) advocates the

protection of representatives of coastal dune populations and inland populations of Corynephorus canescens, wet fen, coastal saltmarsh and lake-edge populations of Hierochloe odorata, Anglesey, Gower and Channel Islands populations of Mibora minima, and so on. Reasoning based on likely differentiation

patterns may sometimes conflict with reasoning based on theories of genetic structure. This may occur with

geographically marginal populations which may be

genetically depauperate (i.e. have low gene diversity)

but may contain heritable adaptations to extreme conditions, say of climate (Gray, 1996c).

The move towards collecting fewer seeds for ex situ conservation, apart from facing the practical realities of limited storage capacity, recognizes what Brown & Briggs (1991) describe as a law of diminishing (genetic) returns in capturing the genetic diversity within a species. They advocate sampling few plants (ten individuals) from each population, arguing that the first ten organisms randomly sampled from a population are as important as, if not more important than, an additional ninety. Whilst suggesting a minimum target of five populations per species, they recognize that the

sample size could be increased, depending on ... the desirability of sampling from a wide range of environments (Brown & Briggs, 1991). Again the environmental axis is deemed the important one. Using a different approach, Lawrence, Marshall & Davies (1995) have shown recently that rather few plants (in fact about 172), sampled at random from a population, are needed to conserve all, or nearly all, of the

polymorphic genes segregating in that population (irrespective of self- or cross-pollination). Furthermore, this number can be divided across populations?thus the sample from each need be no larger than 172 divided by the number of populations. By sampling at random, say, eighteen plants from ten populations, there is a high probability of conserving at least one copy of each allele at nearly all loci?these calculations do not include alleles at frequencies in the target species, or individual population, below 0.05 (the relative

importance of the rare allele in plant breeding is a contentious issue).

The ability to capture most of the genetic diversity within a species' populations by sampling a relatively small number of plants from a wide range of

populations further supports the idea of a habitat- based conservation strategy. For in situ conservation of diversity, the protection of populations across a range of habitat-types must be the important first consideration. Note, this is not the same thing as saying that an optimal in situ conservation strategy would be to preserve many small populations of a species rather than one, or a few, large ones. Other considerations apply to this argument, such as the effects of population size on genetic drift and inbreeding (Barrett & Kohn, 1991).

Finally, even if we build into a generic strategy the

concept of conserving diversity along the environmental axis or gradient, are there no refinements we can make to this rather general paradigm? Are





comparisons between species impossible, or misleading as suggested earlier, because patterns of diversity and structure are otherwise unpredictable?

One approach, that adopted by the Center for Plant Conservation (in Falk & Holsinger, 1991, see also Falk, 1991), is to take account of what is known about the biology of each species and, based on the sort of comparisons drawn by Hamrick and others, decide how many populations should be sampled by the degree of genetic differentiation one might expect to find among them. This is likely to depend on the potential for gene flow among populations and indicates, for example, that an annual, self-fertilizing angiosperm of early successional habitats will be more differentiated (and on the whole should be sampled across more populations) than a long-lived, outbreeding, wind- pollinated gymnosperm of climax communities. In their list of characteristics which should determine the number of populations to be sampled for ex situ conservation, the Center for Plant Conservation gives the highest priority (apart from the imminent destruction of its populations) to species which have high observed ecotypic or site variation. They then list a series of both physical characteristics, such as the degree of isolation of populations, and biological characteristics, such as self-fertilizing, annual life history, and so on (Falk & Holsinger, 1991).

There may be considerable scope for refining such a strategy by adopting a phylogenetic approach to the comparison of genetic structure in species' populations. Comparative methods in biology are currently receiving much attention, particularly in evolutionary ecology, where the debate is fierce (e.g. the Forum section of Journal of Ecology, Vol. 83 (nos. 3, 4 and 5), 1995). At particular issue is the interpretation of patterns of shared species traits and whether accounting for the patterns of relatedness among these species (their phylogenetic background) is a necessary correction (to avoid a form of pseudoreplication) before other comparisons, say those using shared ecological backgrounds, can be made (or whether phylogenetic and ecological perspectives are to some degree independent). Whatever the truth, the insights to be gained from taking a phylogenetic approach to comparative studies are many (Harvey & Pagel, 1991). Species with common genetic backgrounds will have faced many of the environmental challenges of the past armed with similar genetic toolkits. They may have made (and be continuing to make) similar responses.

For example, a simple division of the grass family (whose species largely share the common and


potentially constraining features of herbaceous life- form and wind pollination) into annuals and perennials produces two groups which display many other contrasting ecological and genetic features that affect differentiation patterns (Gray, 1996b). The annuals are more likely to be diploid, inbreeding, r-selected strategists of open, ephemeral habitats?all features which tend to restrict genetic recombination and accelerate the rate of between-population differentiation. The genetic structures of populations of the perennial Agrostis curtisii and the annual Gastridium ventricosum referred to earlier may be an extreme

example of such contrasts, but there is evidence of similarly contrasting patterns in rare grass populations, even in traits under polygenic control (Gray, 1991, 1996b). A comparison of Northern Hemisphere conifer species by Millar & Libby (1991), whilst not explicitly championing a phylogenetic approach, illustrates how patterns of either continuous or discontinuous environmental variation and of variation in population size and degree of isolation, can produce predictable, contrasting patterns of genetic diversity within the same taxonomic group. Such examples suggest that insights into the partitioning of genetic diversity among populations, and hence the basis of the sampling strategy to conserve it, may be gained by applying, to

groups of related species, the lessons of empirical studies across the whole plant kingdom. The unthinkable alternative is to abandon the search for generalizations and embark on the Sisiphean task of measuring genetic diversity in most populations of

every species.

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Genetic Diversity and Its Conservation in Natural Populations of Plants

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