Sergey Gavrilets

PERSPECTIVE: MODELS OF SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS?

Abstract Theoretical studies of speciation have been dominated by numerical simulations aiming to demonstrate that speciation in a certain scenario may occur. What is needed now is a shift in focus to identifying more general rules and patterns in the dynamics of speciation. The crucial step in achieving this goal is the development of simple and general dynamical models that can be studied not only numerically but analytically as well. I review some of the existing analytical results on speciation. I first show why the classical theories of speciation by peak shifts across adaptive valleys driven by random genetic drift run into trouble (and into what kind of trouble). Then I describe the Bateson‐Dobzhansky‐Muller (BDM) model of speciation that does not require overcoming selection. I describe exactly how the probability of speciation, the average waiting time to speciation, and the average duration of speciation depend on the mutation and migration rates, population size, and selection for local adaptation. The BDM model postulates a rather specific genetic architecture of reproductive isolation. I then show exactly why the genetic architecture required by the BDM model should be common in general. Next I consider the multilocus generalizations of the BDM model again concentrating on the qualitative characteristics of speciation such as the average waiting time to speciation and the average duration of speciation. Finally, I consider two models of sympatric speciation in which the conditions for sympatric speciation were found analytically. A number of important conclusions have emerged from analytical studies. Unless the population size is small and the adaptive valley is shallow, the waiting time to a stochastic transition between the adaptive peaks is extremely long. However, if transition does happen, it is very quick. Speciation can occur by mutation and random drift alone with no contribution from selection as different populations accumulate incompatible genes. The importance of mutations and drift in speciation is augmented by the general structure of adaptive landscapes. Speciation can be understood as the divergence along nearly neutral networks and holey adaptive landscapes (driven by mutation, drift, and selection for adaptation to a local biotic and/or abiotic environment) accompanied by the accumulation of reproductive isolation as a by‐product. The waiting time to speciation driven by mutation and drift is typically very long. Selection for local adaptation (either acting directly on the loci underlying reproductive isolation via their pleiotropic effects or acting indirectly via establishing a genetic barrier to gene flow) can significantly decrease the waiting time to speciation. In the parapatric case the average actual duration of speciation is much shorter than the average waiting time to speciation. Speciation is expected to be triggered by changes in the environment. Once genetic changes underlying speciation start, they go to completion very rapidly. Sympatric speciation is possible if disruptive selection and/or assortativeness in mating are strong enough. Sympatric speciation is promoted if costs of being choosy are small (or absent) and if linkage between the loci experiencing disruptive selection and those controlling assortative mating is strong.

Adaptive Radiation: Contrasting Theory with Data

Biologists have long been fascinated by the exceptionally high diversity displayed by some evolutionary groups. Adaptive radiation in such clades is not only spectacular, but is also an extremely complex process influenced by a variety of ecological, genetic, and developmental factors and strongly dependent on historical contingencies. Using modeling approaches, we identify 10 general patterns concerning the temporal, spatial, and genetic/morphological properties of adaptive radiation. Some of these are strongly supported by empirical work, whereas for others, empirical support is more tentative. In almost all cases, more data are needed. Future progress in our understanding of adaptive radiation will be most successful if theoretical and empirical approaches are integrated, as has happened in other areas of evolutionary biology.

The evolution of female mate choice by sexual conflict

Although empirical evidence has shown that many male traits have evolved via sexual selection by female mate choice, our understanding of the adaptive value of female mating preferences is still very incomplete. It has recently been suggested that female mate choice may result from females evolving resistance rather than attraction to males, but this has been disputed. Here, we develop a quantitative genetic model showing that sexual conflict over mating indeed results in the joint evolution of costly female mate choice and exaggerated male traits under a wide range of circumstances. In contrast to traditional explanations of costly female mate choice, which rely on indirect genetic benefits, our model shows that mate choice can be generated as a side–effect of females evolving to reduce the direct costs of mating.

The dynamics of evolutionary stasis

Abstract The fossil record displays remarkable stasis in many species over long time periods, yet studies of extant populations often reveal rapid phenotypic evolution and genetic differentiation among populations. Recent advances in our understanding of the fossil record and in population genetics and evolutionary ecology point to the complex geographic structure of species being fundamental to resolution of how taxa can commonly exhibit both short-term evolutionary dynamics and long-term stasis.

Sympatric speciation by sexual conflict

It is well established that sexual conflict can drive an endless coevolutionary chase between the sexes potentially leading to genetic divergence of isolated populations and allopatric speciation. We present a simple mathematical model that shows that sexual conflict over mating rate can result in two other general regimes. First, rather than “running away” from males, females can diversify genetically into separate groups, effectively “trapping” the males in the middle at a state characterized by reduced mating success. Female diversification brings coevolutionary chase to the end. Second, under certain conditions, males respond to female diversification by diversifying themselves. This response results in the formation of reproductively isolated clusters of genotypes that emerge sympatrically.

20 Questions on Adaptive Dynamics

Adaptive Dynamics is an approach to studying evolutionary change when fitness is density or frequency dependent. Modern papers identifying themselves as using this approach first appeared in the 1990s, and have greatly increased up to the present. However, because of the rather technical nature of many of the papers, the approach is not widely known or understood by evolutionary biologists. In this review we aim to remedy this situation by outlining the methodology and then examining its strengths and weaknesses. We carry this out by posing and answering 20 key questions on Adaptive Dynamics. We conclude that Adaptive Dynamics provides a set of useful approximations for studying various evolutionary questions. However, as with any approximate method, conclusions based on Adaptive Dynamics are valid only under some restrictions that we discuss.

The genetics of phenotypic plasticity. V. Evolution of reaction norm shape

We present a general quantitative genetic model for the evolution of reaction norms. This model goes beyond previous models by simultaneously permitting any shaped reaction norm and allowing for the imposition of genetic constraints. Earlier models are shown to be special cases of our general model; we discuss in detail models involving just two macroenvironments, linear reaction norms, and quadratic reaction norms. The model predicts that, for the case of a temporally varying environment, a population will converge on (1) the genotype with the maximum mean geometric fitness over all environments, (2) a linear reaction norm whose slope is proportional to the covariance between the environment of development and the environment of selection, and (3) a linear reaction norm even if nonlinear reaction norms are possible. An examination of experimental studies finds some limited support for these predictions. We discuss the limitations of our model and the need for more realistic gametic models and additional data on the genetic and developmental bases of plasticity.

PATTERNS OF PARAPATRIC SPECIATION

Abstract. Geographic variation may ultimately lead to the splitting of a subdivided population into reproductively isolated units in spite of migration. Here, we consider how the waiting time until the first split and its location depend on different evolutionary factors including mutation, migration, random genetic drift, genetic architecture, and the geometric structure of the habitat. We perform large‐scale, individual‐based simulations using a simple model of reproductive isolation based on a classical view that reproductive isolation evolves as a by‐product of genetic divergence. We show that rapid parapatric speciation on the time scale of a few hundred to a few thousand generations is plausible even when neighboring subpopulations exchange several individuals each generation. Divergent selection for local adaptation is not required for rapid speciation. Our results substantiates the claims that species with smaller range sizes (which are characterized by smaller local densities and reduced dispersal ability) should have higher speciation rates. If mutation rate is small, local abundances are low, or substantial genetic changes are required for reproductive isolation, then central populations should be the place where most splits take place. With high mutation rates, high local densities, or with moderate genetic changes sufficient for reproductive isolation, speciation events are expected to involve mainly peripheral populations.

Linking the emergence of fungal plant diseases with ecological speciation

Emerging diseases represent a growing worldwide problem accompanying global environmental changes. There is tremendous interest in identifying the factors controlling the appearance and spread of these diseases. Here, we discuss emerging fungal plant diseases, and argue that they often result from host shift speciation (a particular case of ecological speciation). We consider the factors controlling local adaptation and ecological speciation, and show that certain life-history traits of many fungal plant pathogens are conducive for rapid ecological speciation, thus favoring the emergence of novel pathogen species adapted to new hosts. We argue that placing the problem of emerging fungal diseases of plants within the context of ecological speciation can significantly improve our understanding of the biological mechanisms governing the emergence of such diseases.

What, if anything, is sympatric speciation?

Sympatric speciation has always fascinated evolutionary biologists, and for good reason; it pits diversifying selection directly against the tendency of sexual reproduction to homogenize populations. However, different investigators have used different definitions of sympatric speciation and different criteria for diagnosing cases of sympatric speciation. Here, we explore some of the definitions that have been used in empirical and theoretical studies. Definitions based on biogeography do not always produce the same conclusions as definitions based on population genetics. The most precise definitions make sympatric speciation an infinitesimal end point of a continuum. Because it is virtually impossible to demonstrate the occurrence of such a theoretical extreme, we argue that testing whether a case fits a particular definition is less informative than evaluating the biological processes affecting divergence. We do not deny the importance of geographical context for understanding divergence. Rather, we believe this context can be better understood by modelling and measuring quantities, such as gene flow and selection, rather than assigning cases to discrete categories like sympatric and allopatric speciation.