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Gene Genealogies and Population Variation in Plants

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Colloquium Gene genealogies and population variation in plants Barbara A. Schaal* and Kenneth M. Olsen Department of Biology, Washington University, St. Louis, MO 63130 Early in the development of plant evolutionary biology, genetic selection. Morphology, karyotypes, and fitness components are drift, fluctuations in population size, and isolation were identified central traits for understanding evolution and adaptation, but as critical processes that affect the course of evolution in plant they limit which evolutionary processes can be studied. In his species. Attempts to assess these processes in natural populations book, Stebbins discusses such events as fluctuations in popula- became possible only with the development of neutral genetic tion size, random fixation (genetic drift), and isolation as all markers in the 1960s. More recently, the application of historically affecting the process of evolution (see passage quoted above; ref. ordered neutral molecular variation (within the conceptual frame- 1). However, the study of these mechanisms requires markers work of coalescent theory) has allowed a reevaluation of these that are not under selection. microevolutionary processes. Gene genealogies trace the evolu- In the years after the publication of Stebbins’ book, among tionary relationships among haplotypes (alleles) with populations. the first major technical advances in evolutionary biology were Processes such as selection, fluctuation in population size, and the development of protein electrophoresis and the identifi- population substructuring affect the geographical and genealog- cation of allozyme variation in natural populations. Many ical relationships among these alleles. Therefore, examination of allozymes are selectively neutral, and thus, for the first time, these genealogical data can provide insights into the evolutionary evolutionary biologists could attempt to assess the amount of history of a species. For example, studies of Arabidopsis thaliana neutral genetic variation within species as well as its spatial have suggested that this species underwent rapid expansion, with distribution. Plant species were found to vary widely, both in populations showing little genetic differentiation. The new disci- levels of genetic variation and in the apportionment of this pline of phylogeography examines the distribution of allele gene- variation within and among populations. These observations alogies in an explicit geographical context. Phylogeographic stud- spurred researchers to examine the mechanisms underlying the ies of plants have documented the recolonization of European tree process of genetic differentiation in plants. One of the most species from refugia subsequent to Pleistocene glaciation, and such common approaches for doing this analysis has been to look for studies have been instructive in understanding the origin and correlations between the life history characteristics of a species domestication of the crop cassava. Currently, several technical (e.g., mechanisms of pollen and seed dispersal, system of limitations hinder the widespread application of a genealogical mating, and generation length) and patterns of population approach to plant evolutionary studies. However, as these tech- genetic differentiation (2). Neutral allelic variation from allo- nical issues are solved, a genealogical approach holds great prom- zymes also can be used to estimate levels of gene flow among ise for understanding these previously elusive processes in plant populations. The population genetic theory developed by evolution. Wright, Fisher, and Malecot (among others) established that, for a group of populations at equilibrium, the level of genetic n the following succinct statements, G. L. Stebbins presents differentiation is roughly inversely proportional to the level of Iwhat would become the framework for the study of plant interpopulation gene flow per generation. This relationship is evolutionary mechanisms for the next 50 years (1). expressed by Wright’s (3) familiar equation for estimating gene Ϸ ͞ ϩ flow under an island model: FST 1 (4Nem 1), where FST Individual variation, in the form of mutation and gene is the standardized variance in allele frequencies among recombination, exists in all populations;...themolding populations, Ne is the effective population size, and m is the of this raw material... into variation on the level of migration rate. populations by means of natural selection, fluctuation in The use of allozymes has led to more than 30 years of insight population size, random fixation and isolation is suffi- into how plant populations evolve. However, inferring popu- cient to account for all of the differences, both adaptive lation structure solely from allele frequencies has its limita- and non-adaptive, which exist between related races and tions. Allozyme alleles (or their DNA analogs, restriction species.... fragment length polymorphisms, amplified fragment length polymorphisms, and microsatellites) are unordered, meaning The problem of the evolutionist is...evaluating on the that the genealogical pattern of relationships among alleles basis of all available evidence the role which each of cannot be easily inferred. As a result, these data cannot be used these known forces has played in any particular evolu- in directly assessing genetic change over time but rather tionary line.... require indirect approaches based on models that often assume A central thesis of Stebbins’ seminal book, Variation and Evolu- equilibrium conditions. For example, Wright’s equation tioninPlants(1), is the notion that to understand evolution we must (above) for quantifying gene flow under the island model examine its action at the level of populations within species. This assumes that populations have reached an equilibrium be- reasoning may seem obvious to contemporary readers, but at the tween gene flow and random genetic drift. This equilibrium time of Stebbins’ writing, the importance of population-level pro- perspective can be biologically misleading, particularly for cesses for evolution was far from apparent. Stebbins’ elucidation of this connection is one of his most enduring contributions to plant This paper was presented at the National Academy of Sciences colloquium ‘‘Variation and evolutionary biology. Evolution in Plants and Microorganisms: Toward a New Synthesis 50 Years After Stebbins,’’ Fifty years ago, the study of plant evolution was necessarily held January 27–29, 2000, at the Arnold and Mabel Beckman Center in Irvine, CA. concerned with the phenotype, much of which is subject to *To whom reprint requests should be addressed. E-mail: [email protected]. 7024–7029 ͉ PNAS ͉ June 20, 2000 ͉ vol. 97 ͉ no. 13 Downloaded by guest on September 27, 2021 species in which recent history is a major determinant of population structure. We speculate that very few plant species have reached, or will ever reach, a gene flow-drift equilibrium. Many plants, both temperate and tropical, have altered their range subsequent to glaciations in the last 20,000 years, a recent event on an evolutionary time scale. Likewise, many plant species have a metapopulation structure with subpopu- lations continually being colonized, dispersing migrants, and going extinct. Such metapopulations may reach a system-wide equilibrium in which probabilities of extinction and recoloni- zation are constant given enough time, but such a situation is unlikely considering the relatively short time frame of global climatic changes in the past. Equilibrium in plants is for the most part a theoretical construct with little relation to reality. We would argue that the second major development since the publication of Stebbins’ work has been the application of or- dered, genealogical data to the study of population-level pro- cesses. This development, which has begun to reach its potential only in the last decade, was predicated on two major advances, one technical and the other conceptual. The technical advance has been the widespread availability of ordered genetic variation at the intraspecific level, typically in the form of DNA sequence variation or mapped restriction-site data. For such data, muta- tional differences among genetic variants indicate the patterns of relationship among variants. These data therefore provide the raw information needed to reconstruct genealogical relation- ships among alleles (i.e., gene trees). The conceptual advance has been the application of coalescent theory to the study of microevolutionary processes (for a recent review, see ref. 4). For a population of constant size, new alleles are continually arising through mutation, and others are going extinct over successive generations (assuming neutrality). There- fore, the extant alleles of a gene in a population are all derived from (i.e., coalesce to) a single common ancestral allele that existed at some point in the past (Fig. 1). Coalescent theory provides a framework for studying the effects of population-level processes (e.g., population size fluctuations, selection, and gene flow) on the expected time to common ancestry of alleles within a gene tree. The application of gene genealogies to population genetics has allowed the study of population-level processes within a temporal, nonequilibrium framework. Thus, microevo- lution can be studied as a dynamic, historical process, changing over time within a species. COLLOQUIUM At the foundation of all genealogical analyses is the gene tree, which represents the inferred genealogical relationships among alleles
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