物种多样性和遗传多样性的关系

REV I EWS AND SYNTHESES Connections between species diversity and genetic diversity Mark Vellend1* and Monica A. Geber2 1National Center for Ecological Analysis and Synthesis, 735 State Street, Suite 300, Santa Barbara, CA 93101, USA 2Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA *Correspondence and present address: Departments of Botany and Zoology, and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada V6T 1Z4. E-mail: mvellend@interchange.ubc.ca Abstract Species diversity and genetic diversity remain the nearly exclusive domains of community ecology and population genetics, respectively, despite repeated recognition in the literature over the past 30 years of close parallels between these two levels of diversity. Species diversity within communities and genetic diversity within populations are hypothesized to co-vary in space or time because of locality characteristics that influence the two levels of diversity via parallel processes, or because of direct effects of one level of diversity on the other via several different mechanisms. Here, we draw on a wide range of studies in ecology and evolution to examine the theoretical underpinnings of these hypotheses, review relevant empirical literature, and outline an agenda for future research. The plausibility of species diversity–genetic diversity relationships is supported by a variety of theoretical and empirical studies, and several recent studies provide direct, though preliminary support. Focusing on potential connections between species diversity and genetic diversity complements other approaches to synthesis at the ecology– evolution interface, and should contribute to conceptual unification of biodiversity research at the levels of genes and species. Keywords Biodiversity, coexistence, community ecology, drift, genetic diversity, migration, neutral model, population genetics, selection, species diversity. Ecology Letters (2005) 8: 767–781 I N TRODUCT ION Individual organisms within a community may represent different species or different genetic variants within species. The birth, death and movement of individuals determine the dynamics of both populations and communities, and therefore both genetic diversity within populations and species diversity within the community. Species diversity and genetic diversity have traditionally received independent treatment by community ecologists and population genet- icists, respectively, despite repeated recognition in the literature over the past 30 years of potential connections between these two most fundamental levels of biodiversity (Antonovics 1976, 1992, 2003; Harper 1977; Huston 1994; Hairston et al. 1996; Amarasekare 2000; Kassen 2002; Chave 2004). The recent emergence of �community genetics� (Antonovics 1992) as �the study of the interaction between genes within a species and populations of other species in a community� (Agrawal 2003) has revived intense interest in understanding the interplay between ecological and evolu- tionary processes in determining community structure and dynamics. Elucidating the different ways in which species diversity and genetic diversity may be linked promises to help achieve this goal, and to provide a basis for conceptual unification in biodiversity research. Here we review the hitherto loosely associated set of ideas pointing to connec- tions between species diversity and genetic diversity, drawing on basic theory in ecology and evolution to provide a conceptual framework and agenda for research on links between these two levels of biodiversity. Species diversity and genetic diversity may be related in three main ways (Fig. 1); these cases are not mutually exclusive. If locality characteristics (or any common cause) influence the two levels of diversity in a parallel manner (Fig. 1, case I), a positive correlation between them may result. To the extent that genetic variation determines a population’s demographic performance and viability, or that genetic variation in a dominant species determines the biotic environment experienced by the rest of the community, species diversity may be causally influenced by genetic Ecology Letters, (2005) 8: 767–781 doi: 10.1111/j.1461-0248.2005.00775.x �2005 Blackwell Publishing Ltd/CNRS diversity within component species (case II). Conversely, if the species diversity of a community influences the selection regime experienced by component populations, genetic diversity may be causally influenced by the diversity and relative abundances of coexisting species (case III). These simple depictions belie a tremendous degree of complexity in the details of how species diversity and genetic diversity may be related. In this paper, we outline the theoretical underpinnings of each of the three general hypotheses, highlighting relevant empirical studies, gaps in our know- ledge and key observations or experiments needed to fill these gaps. A vast literature falls under the general themes of species and genetic diversity. A narrowing of scope is therefore needed to restrict attention to the key points of contact between the two levels of diversity. First, we will consider only �local� diversity measured in patches of habitat or experimental plots (�localities�) within a single region. In the framework presented here, genetic diversity within particular species must be measured or manipulated in different localities; when considering diversity patterns at large spatial scales (e.g. latitudinal gradients), this is not possible even in theory because variation in species diversity is often accompanied by complete turnover in species composition (i.e. none of the species can be sampled in all localities). Second, at the community level, we only consider diversity within a single trophic level. Different genotypes of the same species may interact in much the same way as different species within a trophic level, but there is no population- level analogue for multitrophic interactions, except perhaps in the special case of cannibalism. Additional constraints that define our domain of application are presented in subsequent sections. Following Chase & Leibold (2003), we use the Tilman (1982) resource competition model in several sections for the purpose of graphical illustration of theoretical concepts. Our conceptual framework is not limited to communities in which resource competition controls dynamics, but this model provides an intuitively straightforward basis for illustrating selected examples. DEF IN I T IONS Species diversity and genetic diversity can be defined, measured or manipulated in a number of different ways. Species diversity is most often measured as species richness, the number of species in a given locality. In studies that experimentally manipulate species diversity (reviewed by Loreau et al. 2001), it is also most often species richness that is varied among treatments. Several indices of species diversity incorporate information about the relative abun- dances of species in a locality, with higher diversity indicated by a more even distribution of abundance among species – higher �evenness� (Magurran 2004). This paper is concerned largely with species richness. When discrete alleles or genotypes can be distinguished in a population, as in studies employing molecular markers, measurements of genetic diversity are closely analogous to those of species diversity. Allelic or genotypic richness is the number of different alleles or genotypes, respectively, in a population. The probability that two randomly chosen alleles or genotypes are different is equivalent to the Hardy– Weinberg expected heterozygosity when estimated for loci in the nuclear genome of diploid organisms, and is also referred to as �gene diversity� for other kinds of genetic markers (Nei 1987). Gene diversity is identical to the Simpson index of species diversity (Magurran 2004). With DNA sequence data, nucleotide diversity (p) is the equivalent of gene diversity for individual nucleotide positions rather than loci, and nucleotide polymorphism (h) is the proportion of nucleotide positions that are variable, or segregating, in a sample of sequences. For quantitative traits, genetic diversity is measured as the genetic variance, or the component of the total phenotypic variance in a population attributable to genetic differences Locality Characteristics Area isolation spatial/temporal heterogeneity environment, etc. Genetic diversity within populations Species diversity within communities Immig ration drift selec tion Immigrationdriftselection Parallel effects (case I) Causal effects Case II Case III Figure 1 Potential connections between species diversity and genetic diversity. 768 M. Vellend and M. A. Geber �2005 Blackwell Publishing Ltd/CNRS among individuals (Falconer & Mackay 1996). The relative magnitude of quantitative genetic variance in large numbers of populations of the same species is reported far less frequently than genetic diversity at loci with discretely recognizable variants (e.g. molecular markers), and is also quite difficult to manipulate experimentally (we return to the latter issue later in this paper.) For this reason, our arguments in this paper pertain largely to genetic diversity measured using discrete alleles or genotypes, although it is important to note that the component of quantitative genetic variance that is inherited additively is directly related to heterozygosity at the underlying loci (Falconer & Mackay 1996). Genetic diversity can be measured for traits that are neutral (often assumed for molecular markers) or traits that are under selection. This distinction has important implica- tions for predicting either the effects of different processes on genetic diversity, or the effects of genetic diversity on population or community characteristics. These differences are highlighted in the Theoretical underpinnings section below. For natural or experimental populations comprised of clonal, non-recombining genotypes, as in many populations of bacteria, zooplankton and clonal or apomictic plants (at least over short periods of time), the measurement and manipulation of genetic diversity is exactly analogous to that of species diversity. For simplicity, our theoretical illustrations using the resource competition model consider genetic diversity as the number of clonal genotypes in a given species. We consider cases in which the interest is in genetic diversity in one particular focal species, and also cases in which the interest is in genetic diversity in each of two or more competing species, although in most empirical studies genetic diversity is measured in only one species from the community. In all cases, we are interested in genetic diversity within populations of parti- cular species. THEORET I CAL UNDERP INN INGS Parallel processes – case I Theories of species diversity and genetic diversity share many striking similarities, to the point that individual models are often described as applying equally well to both (e.g. Amarasekare 2000; Chase & Leibold 2003). Empirical data have revealed a predominance of positive relationships between species diversity and genetic diversity (see section Empirical research past and future), and here we focus on potential processes acting in parallel at the two levels that may create such relationships in the absence of direct causal effects of one level of diversity on the other. Genetic diversity is controlled by four processes, mutation, drift, migration and selection, each of which has an analogue at the level of species diversity (Table 1). Speciation creates new species much as mutation creates new alleles. However, because speciation and mutation occur on very different time scales and speciation is unlikely to explain variation in diversity among localities within a region (but see Losos & Schluter 2000), we restrict our attention to the remaining three processes, which may create variation in diversity among localities in very similar ways at the two levels. Drift and migration As a necessary consequence of populations and commu- nities being comprised of finite numbers of individuals, both genes and species are prone to random fluctuations in abundance (i.e. drift), possibly to the point of local extinction. Immigration may provide new species or novel alleles at one or more loci that counteract the effects of drift. Drift and migration influence species and genetic diversity in fairly similar and straightforward ways (but see section Caveats). Neutral diversity is regulated almost entirely by the action of drift and migration (plus mutation and speciation; Kimura 1983; Hubbell 2001), but these processes can also have important effects on non-neutral diversity (e.g. Lenormand 2002; Mouquet et al. 2004; Vellend 2005). The effects of drift and migration are frequently manifested as positive correlations of diversity with the area or connec- tivity of localities (Rosenzweig 1995; Frankham et al. 2002), and these variable locality characteristics may, in turn, drive positive correlations between species diversity and genetic diversity (Vellend 2005). Selection and environmental heterogeneity The influence of selective processes on diversity is considerably more complex than that of neutral processes. Only non-neutral genetic diversity is relevant here, except to the extent that selection may alter overall population size, Table 1 Processes that influence diversity, defined to emphasize the parallels at the levels of genetic diversity and species diversity Mutation/speciation: the creation of new alleles/species Drift: random changes in the relative frequencies of alleles/species Migration: movement among populations/communities of alleles/species Selection: processes that favour particular alleles/species over others Species diversity and genetic diversity 769 �2005 Blackwell Publishing Ltd/CNRS and therefore genetic diversity for neutral traits as well. At the most basic level, selection favours some individuals over others and these individuals may represent different species or different genetic variants within species. There are far too many selection-based theories of diversity in community ecology to deal with individually, so to determine which theories may be relevant to explaining correlated patterns of species and genetic diversity, it is useful here to highlight the subtle distinction between models of species coexistence, and models of diversity patterns in space or time. Studies of coexistence generally aim to discover processes that prevent one type dominating all others (Gause 1934). As such, models of coexistence are often applied to understanding community dynamics at a single locality, and may or may not help explain why one place has more diversity than another. In the context of this review, the only mechanisms of coexistence that need be considered are those in which the strength of the underlying process varies among localities. As will be explained below, for some mechanisms this is plausible, while for others it is not. Spatial and temporal heterogeneity in the environment may create diversifying selection that is thought to be a powerful mechanism of maintaining both species diversity and genetic diversity and so may generate correlations between them. Different species or genotypes can coexist if species- or genotype-specific fitness varies in space or time such that each type is favoured over the others in enough places or at enough times to avoid local extinction in the long term (Chesson 2000; Barot & Gignoux 2004). The spatial or temporal environmental heterogeneity can be of two general types. Exogenous heterogeneity includes spatial or temporal variation in factors such as soil characteristics or climate. Such heterogeneity is ubiquitous in nature (Bell et al. 1993), and because localities may vary in the magnitude of internal heterogeneity, they may also differ in diversity (e.g. Tews et al. 2004). Endogenous heterogeneity arises from the activities of organisms themselves. For example, if some species or genotypes have high survival rates in the face of competition but low colonization rates of newly opened microsites, or vice versa, coexistence of many species is possible (Tilman 1994). However, given the same potential species pool in different localities, it is difficult to imagine how the strength of such a process could vary among localities in such a way as to drive patterns of species and genetic diversity in predictable and parallel ways, even though colonization–competition tradeoffs may operate both within (e.g. Solbrig & Simpson 1974) and among species (Tilman 1994). On the other hand, if spatial or temporal variability in the identity of neighbours (i.e. competitors) is considered a source of endogenous heterogeneity (Huston & DeAngelis 1994), the potential arises for direct effects of one level of diversity on the other. This potential is addressed in subsequent sections. Simultaneous responses of species diversity and genetic diversity The preceding discussion points to three variable locality characteristics as strong candidates for having parallel effects on, and creating correlated patterns in, species diversity and genetic diversity. Locality area influences both levels of diversity via drift; isolation via immigration; and exogenous heterogeneity via spatially or temporally varying selection. We do not consider variation among localities in average environmental quality (e.g. producti- vity and soil moisture) to be a likely driver of parallel variation in species and genetic diversity. Although average environmental conditions are often strong predictors of diversity, the underlying mechanisms are likely to vary among systems (e.g. Waide et al. 1999), and each species is likely to respond individualistically to the environment, so we cannot make any general predictions about parallel effects on species and genetic diversity. This represents an important limit to the domain of application of the present approach. While the factors that influence species diversity and genetic diversity in isolation have received thorough theoretical treatment, relatively little is known about the simultaneous response of the two levels of diversity to variable locality characteristics. Figure 2 illustrates one scenario in which environmental heterogeneity may increase both species diversity and genetic diversity when species and genotypes compete for resources. A recent modelling study of both levels of diversity under a range of scenarios produced some results that adhere to expectations based on separate community and population models, while other results were more surprising (Vellend 2005). In this individual-based and spatially explicit simulation model of plant communities, locality area and immigration rate had universal positive effects on both species diversity and genetic diversity, regardless of whether or not variants were neutral with respect to selection (Vellend 2005). Area and isolation drove positive correlations between species diver- sity and genetic diversity and the correlations were stronger when genetic diversity was measured for common vs. rare species. In these models, spatial environmental heterogen- eity always had a strong positive effect on species diversity by allowing coexistence of species with fitness optima at different positions along an environmental gradient. How- ever, although genotypes differed within species in much the same way that species differed within the community, the effects of environmental