The origin of biological diversity, via the formation of new species, can be inextricably linked to adaptation to the ecological environment. Specifically, ecological processes are central to the ...formation of new species when barriers to gene flow (reproductive isolation) evolve between populations as a result of ecologically based divergent natural selection. This process of ‘ecological speciation’ has seen a large body of focused research in the last ten-fifteen years, and a review and synthesis of the theoretical and empirical literature is now timely. The book begins by clarifying what ecological speciation is, its alternatives, and the predictions that can be used to test for it. It then reviews the three components of ecological speciation and discusses the geography and genomic basis of the process. A final chapter highlights future research directions, describing the approaches and experiments which might be used to conduct that future work. The ecological and genetic literature is integrated throughout the text with the goal of shedding new insight into the speciation process, particularly when the empirical data is then further integrated with theory.
Theoretical and empirical studies have demonstrated that divergent natural selection can promote the evolution of reproductive isolation. Three unresolved questions concern the types of reproductive ...barriers involved, the role of geography, and the factors determining the extent of progress toward complete speciation. Here I synthesize studies of Timema cristinae host plant ecotypes to address these issues. The approach is to compare the magnitude of multiple reproductive barriers among different ecological and geographic scenarios, where pairs of populations within each scenario are the unit of replication. Application of this approach to T. cristinae revealed that divergent host adaptation can promote the evolution of diverse reproductive barriers, including those that are not inherently ecological. Gene flow in parapatry tended to constrain divergence, with the notable exception of the reinforcement of sexual isolation. Thus, geography affected progress toward speciation but did not influence all reproductive barriers in the same way. Studies of any single pair of taxa often capture only certain stages of the speciation process. For example, reproductive isolation between T. cristinae ecotypes is incomplete, and so only the stages before the completion of speciation have been examined. Studies of more divergent taxa within the genus are required to determine the factors that complete speciation.
A remarkable suite of forms of genomic conflict has recently been implicated in speciation. We propose that these diverse roles of genomic conflict in speciation processes can be unified using the ...concept of ‘conflictual speciation’. Conflictual speciation centers on the evolution of reproductive isolation as a byproduct of antagonistic selection among genomic elements with divergent fitness interests. Intragenomic conflicts are expected to readily generate Dobzhansky–Muller incompatibilities, due to population-specific interactions between opposing elements, and thus they could be especially important in speciation. Moreover, selection from genomic conflicts should be relatively unrelenting across ecological and evolutionary time scales. We explain how intragenomic conflicts can promote, or sometimes constrain, speciation, and describe evidence relating conflicts to the evolution of reproductive isolation.
Speciation is a fundamental process responsible for the diversity of life. Progress has been made in detecting individual ‘speciation genes’ that cause reproductive isolation. In contrast, until ...recently, less attention has been given to genome-wide patterns of divergence during speciation. Thus, major questions remain concerning how individual speciation genes are arrayed within the genome, and how this affects speciation. This theme issue is dedicated to exploring this genomic perspective of speciation. Given recent sequencing and computational advances that now allow genomic analyses in most organisms, the goal is to help move the field towards a more integrative approach. This issue draws upon empirical studies in plants and animals, and theoretical work, to review and further document patterns of genomic divergence. In turn, these studies begin to disentangle the role that different processes, such as natural selection, gene flow and recombination rate, play in generating observed patterns. These factors are considered in the context of how genomes diverge as speciation unfolds, from beginning to end. The collective results point to how experimental work is now required, in conjunction with theory and sequencing studies, to move the field from descriptive studies of patterns of divergence towards a predictive framework that tackles the causes and consequences of genome-wide patterns.
Ecological speciation Rundle, Howard D.; Nosil, Patrik
Ecology letters,
March 2005, Volume:
8, Issue:
3
Journal Article
Peer reviewed
Ecological processes are central to the formation of new species when barriers to gene flow (reproductive isolation) evolve between populations as a result of ecologically‐based divergent selection. ...Although laboratory and field studies provide evidence that ‘ecological speciation’ can occur, our understanding of the details of the process is incomplete. Here we review ecological speciation by considering its constituent components: an ecological source of divergent selection, a form of reproductive isolation, and a genetic mechanism linking the two. Sources of divergent selection include differences in environment or niche, certain forms of sexual selection, and the ecological interaction of populations. We explore the evidence for the contribution of each to ecological speciation. Forms of reproductive isolation are diverse and we discuss the likelihood that each may be involved in ecological speciation. Divergent selection on genes affecting ecological traits can be transmitted directly (via pleiotropy) or indirectly (via linkage disequilibrium) to genes causing reproductive isolation and we explore the consequences of both. Along with these components, we also discuss the geography and the genetic basis of ecological speciation. Throughout, we provide examples from nature, critically evaluate their quality, and highlight areas where more work is required.
Classic debates concerning the extent to which scientists can predict evolution have gained new urgency as environmental changes force species to adapt or risk extinction. We highlight how our ...ability to predict evolution can be constrained by data limitations that cause poor understanding of deterministic natural selection. We then emphasize how such data limits can be reduced with feasible empirical effort involving a combination of approaches.
Divergent natural selection has been shown to promote speciation in many taxa. However, although divergent selection often initiates the process of speciation, it often fails to complete it. Several ...time-based, geographic and genetic factors have been recognized to explain this variability in how far speciation proceeds. We review here recent evidence indicating that variability in the completeness of speciation can also be associated with the nature of divergent selection itself, with speciation being greatly promoted by (i) stronger selection on a given, single trait (the ‘stronger selection’ hypothesis) and (ii) selection on a greater number of traits (the ‘multifarious selection’ hypothesis). However, evidence for each selective hypothesis is still scarce, and further work is required to determine their relative importance.
Levels of genetic differentiation between populations can be highly variable across the genome, with divergent selection contributing to such heterogeneous genomic divergence. For example, loci under ...divergent selection and those tightly physically linked to them may exhibit stronger differentiation than neutral regions with weak or no linkage to such loci. Divergent selection can also increase genome-wide neutral differentiation by reducing gene flow (e.g. by causing ecological speciation), thus promoting divergence via the stochastic effects of genetic drift. These consequences of divergent selection are being reported in recently accumulating studies that identify: (i) 'outlier loci' with higher levels of divergence than expected under neutrality, and (ii) a positive association between the degree of adaptive phenotypic divergence and levels of molecular genetic differentiation across population pairs 'isolation by adaptation' (IBA). The latter pattern arises because as adaptive divergence increases, gene flow is reduced (thereby promoting drift) and genetic hitchhiking increased. Here, we review and integrate these previously disconnected concepts and literatures. We find that studies generally report 5-10% of loci to be outliers. These selected regions were often dispersed across the genome, commonly exhibited replicated divergence across different population pairs, and could sometimes be associated with specific ecological variables. IBA was not infrequently observed, even at neutral loci putatively unlinked to those under divergent selection. Overall, we conclude that divergent selection makes diverse contributions to heterogeneous genomic divergence. Nonetheless, the number, size, and distribution of genomic regions affected by selection varied substantially among studies, leading us to discuss the potential role of divergent selection in the growth of regions of differentiation (i.e. genomic islands of divergence), a topic in need of future investigation.
Speciation is often viewed as a continuum along which populations diverge until they become reproductively-isolated species. However, such divergence may be heterogeneous, proceeding in fits and ...bursts, rather than being uniform and gradual. We show in Timema stick insects that one component of reproductive isolation evolves non-uniformly across this continuum, whereas another does not. Specifically, we use thousands of host-preference and mating trials to study habitat and sexual isolation among 42 pairs of taxa spanning a range of genomic differentiation and divergence time. We find that habitat isolation is uncoupled from genomic differentiation within species, but accumulates linearly with it between species. In contrast, sexual isolation accumulates linearly across the speciation continuum, and thus exhibits similar dynamics to morphological traits not implicated in reproductive isolation. The results show different evolutionary dynamics for different components of reproductive isolation and highlight a special relevance for species status in the process of speciation.
Predicting evolution remains difficult. We studied the evolution of cryptic body coloration and pattern in a stick insect using 25 years of field data, experiments, and genomics. We found that ...evolution is more difficult to predict when it involves a balance between multiple selective factors and uncertainty in environmental conditions than when it involves feedback loops that cause consistent back-and-forth fluctuations. Specifically, changes in color-morph frequencies are modestly predictable through time (
= 0.14) and driven by complex selective regimes and yearly fluctuations in climate. In contrast, temporal changes in pattern-morph frequencies are highly predictable due to negative frequency-dependent selection (
= 0.86). For both traits, however, natural selection drives evolution around a dynamic equilibrium, providing some predictability to the process.
PDF
