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Species formation is a central topic in biology, and a large body of theoretical work has explored the conditions under which speciation occurs, including whether speciation dynamics are gradual or abrupt. In some cases of abrupt speciation, differentiation slowly builds up until it reaches a threshold, at which point linkage disequilibrium (LD) and divergent selection enter a positive feedback loop that triggers accelerated change. Notably, such abrupt transitions powered by a positive feedback have also been observed in a range of other systems. Efforts to anticipate abrupt transitions have led to the development of "early warning signals" (EWS), that is, specific statistical patterns preceding abrupt transitions. Examples of EWS are rising autocorrelation and variance in time-series data due to the reduction of the ability of the system to recover from disturbances. Here, we investigate whether speciation dynamics in theoretical models also exhibit EWS. Using a model of genetic divergence between two populations, we search for EWS before gradual and abrupt speciation events. We do so using six different metrics of differentiation: the effective migration rate, the number of selected loci, the mean fitness of our studied population, LD, FST, and Dabs, a metric analogous to DXY. We find evidence for EWS, with a heterogeneity in their strength among differentiation metrics. We specifically identify FST and the effective migration rate as the most reliable EWS of upcoming abrupt speciation events. Our results provide initial insights into potential EWS of impending speciation and contribute to efforts to generalize the mechanisms underlying EWS., (© The Author(s) 2023. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).)

The concept of a "speciation continuum" has gained popularity in recent decades. It emphasizes speciation as a continuous process that may be studied by comparing contemporary population pairs that show differing levels of divergence. In their recent perspective article in Evolution, Stankowski and Ravinet provided a valuable service by formally defining the speciation continuum as a continuum of reproductive isolation, based on opinions gathered from a survey of speciation researchers. While we agree that the speciation continuum has been a useful concept to advance the understanding of the speciation process, some intrinsic limitations exist. Here, we advocate for a multivariate extension, the speciation hypercube, first proposed by Dieckmann et al. in 2004, but rarely used since. We extend the idea of the speciation cube and suggest it has strong conceptual and practical advantages over a one-dimensional model. We illustrate how the speciation hypercube can be used to visualize and compare different speciation trajectories, providing new insights into the processes and mechanisms of speciation. A key strength of the speciation hypercube is that it provides a unifying framework for speciation research, as it allows questions from apparently disparate subfields to be addressed in a single conceptual model., (© The Author(s) 2022. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE). All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Speciation is a fundamental process shaping biodiversity. However, existing empirical methods often cannot provide key genetic and functional details required to validate speciation theory. New gene modification technologies can verify the causal functionality of genes with astonishing accuracy, helping resolve questions about how reproductive isolation evolves during speciation., (Copyright © 2020 Elsevier Ltd. All rights reserved.)

Studies assessing the predictability of evolution typically focus on short-term adaptation within populations or the repeatability of change among lineages. A missing consideration in speciation research is to determine whether natural selection predictably transforms standing genetic variation within populations into differences between species. Here, we test whether and how host-related selection on diapause timing associates with genome-wide differentiation during ecological speciation by comparing ancestral hawthorn and newly formed apple-infesting host races of Rhagoletis pomonella to their sibling species Rhagoletis mendax that attacks blueberries. The associations of 57 857 single nucleotide polymorphisms in a diapause genome-wide-association study (GWAS) on the hawthorn race strongly predicted the direction and magnitude of genomic divergence among the three fly populations at a field site in Fennville, MI, USA. The apple race and R. mendax show parallel changes in the frequencies of putative inversions on three chromosomes associated with the earlier fruiting times of apples and blueberries compared to hawthorns. A diapause GWAS on R. mendax revealed compensatory changes throughout the genome accounting for the earlier eclosion of blueberry, but not apple flies. Thus, a degree of predictability, although not complete, exists in the genomics of diapause across the ecological speciation continuum in Rhagoletis . The generality of this result is placed in the context of other similar systems. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Speciation with gene flow may require adaptive divergence of multiple traits to generate strong ecologically based reproductive isolation. Extensive negative pleiotropy or physical linkage of genes in the wrong phase affecting these diverging traits may therefore hinder speciation, while genetic independence or "modularity" among phenotypic traits may reduce constraints and facilitate divergence. Here, we test whether the genetics underlying two components of diapause life history, initial diapause intensity and diapause termination timing, constrain differentiation between sympatric hawthorn and apple-infesting host races of the fly Rhagoletis pomonella through analysis of 10,256 SNPs measured via genotyping-by-sequencing (GBS). Loci genetically associated with diapause termination timing were mainly observed for SNPs mapping to chromosomes 1-3 in the genome, most notably for SNPs displaying higher levels of linkage disequilibrium (LD), likely due to inversions. In contrast, selection on initial diapause intensity affected loci on all five major chromosomes of the genome, specifically those showing low levels of LD. This lack of overlap in genetically associated loci suggests that the two diapause phenotypes are largely modular. On chromosome 2, however, intermediate level LD loci and a subgroup of high LD loci displayed significant negative relationships between initial diapause intensity and diapause termination time. These gene regions on chromosome 2 therefore affected both traits, while most regions were largely independent. Moreover, loci associated with both measured traits also tended to exhibit highly divergent allele frequencies between the host races. Thus, the presence of nonoverlapping genetic modules likely facilitates simultaneous, adaptive divergence for the measured life-history components., (© 2017 John Wiley & Sons Ltd.)

The study of ecological speciation is inherently linked to the study of selection. Methods for estimating phenotypic selection within a generation based on associations between trait values and fitness (e.g. survival) of individuals are established. These methods attempt to disentangle selection acting directly on a trait from indirect selection caused by correlations with other traits via multivariate statistical approaches (i.e. inference of selection gradients). The estimation of selection on genotypic or genomic variation could also benefit from disentangling direct and indirect selection on genetic loci. However, achieving this goal is difficult with genomic data because the number of potentially correlated genetic loci (p) is very large relative to the number of individuals sampled (n). In other words, the number of model parameters exceeds the number of observations (p ≫ n). We present simulations examining the utility of whole-genome regression approaches (i.e. Bayesian sparse linear mixed models) for quantifying direct selection in cases where p ≫ n. Such models have been used for genome-wide association mapping and are common in artificial breeding. Our results show they hold promise for studies of natural selection in the wild and thus of ecological speciation. But we also demonstrate important limitations to the approach and discuss study designs required for more robust inferences., (© 2016 John Wiley & Sons Ltd.)

Background: Replicate population pairs that diverge in response to similar selective regimes allow for an investigation of (a) whether phenotypic traits diverge in a similar and predictable fashion, (b) whether there is gradual variation in phenotypic divergence reflecting variation in the strength of natural selection among populations, (c) whether the extent of this divergence is correlated between multiple character suites (i.e., concerted evolution), and (d) whether gradual variation in phenotypic divergence predicts the degree of reproductive isolation, pointing towards a role for adaptation as a driver of (ecological) speciation. Here, we use poeciliid fishes of the genera Gambusia and Poecilia that have repeatedly evolved extremophile lineages able to tolerate high and sustained levels of toxic hydrogen sulfide (H2S) to answer these questions., Results: We investigated evolutionary divergence in response to H2S in Gambusia spp. (and to a lesser extent Poecilia spp.) using a multivariate approach considering the interplay of life history, body shape, and population genetics (nuclear miscrosatellites to infer population genetic differentiation as a proxy for reproductive isolation). We uncovered both shared and unique patterns of evolution: most extremophile Gambusia predictably evolved larger heads and offspring size, matching a priori predictions for adaptation to sulfidic waters, while variation in adult life histories was idiosyncratic. When investigating patterns for both genera (Gambusia and Poecilia), we found that divergence in offspring-related life histories and body shape were positively correlated across populations, but evidence for individual-level associations between the two character suites was limited, suggesting that genetic linkage, developmental interdependencies, or pleiotropic effects do not explain patterns of concerted evolution. We further found that phenotypic divergence was positively correlated with both environmental H2S-concentration and neutral genetic differentiation (a proxy for gene flow)., Conclusions: Our results suggest that higher toxicity exerts stronger selection, and that divergent selection appears to constrain gene flow, supporting a scenario of ecological speciation. Nonetheless, progress toward ecological speciation was variable, partially reflecting variation in the strength of divergent selection, highlighting the complexity of selective regimes even in natural systems that are seemingly governed by a single, strong selective agent.

The interplay between selection and aspects of the genetic architecture of traits (such as linkage, dominance, and epistasis) can either drive or constrain speciation [1-3]. Despite accumulating evidence that speciation can progress to "intermediate" stages-with populations evolving only partial reproductive isolation-studies describing selective mechanisms that impose constraints on speciation are more rare than those describing drivers. The stick insect Timema cristinae provides an example of a system in which partial reproductive isolation has evolved between populations adapted to different host plant environments, in part due to divergent selection acting on a pattern polymorphism [4, 5]. Here, we demonstrate how selection on a green/melanistic color polymorphism counteracts speciation in this system. Specifically, divergent selection between hosts does not occur on color phenotypes because melanistic T. cristinae are cryptic on the stems of both host species, are resistant to a fungal pathogen, and have a mating advantage. Using genetic crosses and genome-wide association mapping, we quantify the genetic architecture of both the pattern and color polymorphism, illustrating their simple genetic control. We use these empirical results to develop an individual-based model that shows how the melanistic phenotype acts as a "genetic bridge" that increases gene flow between populations living on different hosts. Our results demonstrate how variation in the nature of selection acting on traits, and aspects of trait genetic architecture, can impose constraints on both local adaptation and speciation., (Copyright © 2015 Elsevier Ltd. All rights reserved.)

Theory predicts that speciation-with-gene-flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome-wide impacts of host-associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation-with-gene-flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co-occurring apple and hawthorn flies in nature. This striking genome-wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco-evolutionary dynamics and genome divergence., (© 2015 The Authors Ecology Letters published by John Wiley & Sons Ltd and CNRS.)

Adaptive radiation (AR) is a key process in the origin of organismal diversity. However, the evolution of trait disparity in connection with ecological specialization is still poorly understood. Available models for vertebrate ARs predict that diversification occurs in the form of temporal stages driven by different selective forces. Here, we investigate the AR of cichlid fishes in East African Lake Tanganyika and use macroevolutionary model fitting to evaluate whether diversification happened in temporal stages. Six trait complexes, for which we also provide evidence of their adaptiveness, are analysed with comparative methods: body shape, pharyngeal jaw shape, gill raker traits, gut length, brain weight and body coloration. Overall, we do not find strong evidence for the 'stages model' of AR. However, our results suggest that trophic traits diversify earlier than traits implicated in macrohabitat adaptation and that sexual communication traits (i.e. coloration) diversify late in the radiation., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

A long-standing problem in evolutionary biology has been determining whether and how gradual, incremental changes at the gene level can account for rapid speciation and bursts of adaptive radiation. Using genome-scale computer simulations, we extend previous theory showing how gradual adaptive change can generate nonlinear population transitions, resulting in the rapid formation of new, reproductively isolated species. We show that these transitions occur via a mechanism rooted in a basic property of biological heredity: the organization of genes in genomes. Genomic organization of genes facilitates two processes: (i) the build-up of statistical associations among large numbers of genes and (ii) the action of divergent selection on persistent combinations of alleles. When a population has accumulated a critical amount of standing, divergently selected variation, the combination of these two processes allows many mutations of small effect to act synergistically and precipitously split one population into two discontinuous, reproductively isolated groups. Periods of allopatry, chromosomal linkage among loci, and large-effect alleles can facilitate this process under some conditions, but are not required for it. Our results complement and extend existing theory on alternative stable states during population divergence, distinct phases of speciation and the rapid emergence of multilocus barriers to gene flow. The results are thus a step towards aligning population genomic theory with modern empirical studies., (© 2014 John Wiley & Sons Ltd.)

Natural selection can drive the repeated evolution of reproductive isolation, but the genomic basis of parallel speciation remains poorly understood. We analyzed whole-genome divergence between replicate pairs of stick insect populations that are adapted to different host plants and undergoing parallel speciation. We found thousands of modest-sized genomic regions of accentuated divergence between populations, most of which are unique to individual population pairs. We also detected parallel genomic divergence across population pairs involving an excess of coding genes with specific molecular functions. Regions of parallel genomic divergence in nature exhibited exceptional allele frequency changes between hosts in a field transplant experiment. The results advance understanding of biological diversification by providing convergent observational and experimental evidence for selection's role in driving repeatable genomic divergence., (Copyright © 2014, American Association for the Advancement of Science.)

Our current understanding of speciation is often based on considering a relatively small number of genes, sometimes in isolation of one another. Here, we describe a possible emergent genome process involving the aggregate effect of many genes contributing to the evolution of reproductive isolation across the speciation continuum. When a threshold number of divergently selected mutations of modest to low fitness effects accumulate between populations diverging with gene flow, nonlinear transitions can occur in which levels of adaptive differentiation, linkage disequilibrium, and reproductive isolation dramatically increase. In effect, the genomes of the populations start to "congeal" into distinct entities representing different species. At this stage, reproductive isolation changes from being a characteristic of specific, divergently selected genes to a property of the genome. We examine conditions conducive to such genome-wide congealing (GWC), describe how to empirically test for GWC, and highlight a putative empirical example involving Rhagoletis fruit flies. We conclude with cautious optimism that the models and concepts discussed here, once extended to large numbers of neutral markers, may provide a framework for integrating information from genome scans, selection experiments, quantitative trait loci mapping, association studies, and natural history to develop a deeper understanding of the genomics of speciation., (© The American Genetic Association. 2014. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

A major issue in evolutionary biology is explaining patterns of differentiation observed in population genomic data, as divergence can be due to both direct selection on a locus and genetic hitchhiking. "Divergence hitchhiking" (DH) theory postulates that divergent selection on a locus reduces gene flow at physically linked sites, facilitating the formation of localized clusters of tightly linked, diverged loci. "Genome hitchhiking" (GH) theory emphasizes genome-wide effects of divergent selection. Past theoretical investigations of DH and GH focused on static snapshots of divergence. Here, we used simulations assessing a variety of strengths of selection, migration rates, population sizes, and mutation rates to investigate the relative importance of direct selection, GH, and DH in facilitating the dynamic buildup of genomic divergence as speciation proceeds through time. When divergently selected mutations were limiting, GH promoted divergence, but DH had little measurable effect. When populations were small and divergently selected mutations were common, DH enhanced the accumulation of weakly selected mutations, but this contributed little to reproductive isolation. In general, GH promoted reproductive isolation by reducing effective migration rates below that due to direct selection alone, and was important for genome-wide "congealing" or "coupling" of differentiation (F(ST)) across loci as speciation progressed., (© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.)

Studies of related populations varying in their degrees of reproductive isolation can provide insights into speciation. Here, the transition from partially isolated host races to more fully separated sibling species is investigated by comparing patterns of genetic differentiation between recently evolved (∼150 generations) apple and ancestral hawthorn-infesting populations of Rhagoletis pomonella to their sister taxon, the undescribed flowering dogwood fly attacking Cornus florida. No fixed or diagnostic private alleles differentiating the three populations were found at any of 23 microsatellites and 10 allozymes scored. Nevertheless, allele frequency differences were sufficient across loci for flowering dogwood fly populations from multiple localities to form a diagnosable genotypic cluster distinct from apple and hawthorn flies, indicative of species status. Genome-wide patterns of differentiation were correlated between the host races and species pair comparisons along the majority of chromosomes, suggesting that similar disruptive selection pressures affect most loci. However, differentiation was more pronounced, with some additional regions showing elevated divergence, for the species pair comparison. Our results imply that Rhagoletis sibling species such as the flowering dogwood fly represent host races writ large, with the transition to species status primarily resulting from increased divergence of the same regions separating apple and hawthorn flies., (© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.)

Studies of patterns of differentiation across genomes are accumulating, yet integrative work that combines approaches and fully capitalizes on new technologies to test explicit hypotheses is still rare. Thus, debates persist about the rate, magnitude, and causes of genomic change. This special section is devoted to helping resolve these debates. The eight studies contained within demonstrate how we can begin to move away from vague metaphors toward quantitative and more precise descriptors of patterns of genetic architecture and divergence. However, a particular genomic pattern can often arise via different combinations of various processes such as selection, gene flow, recombination, mutation, genetic drift, and demographic variability. Thus, substantial challenges remain in elucidating which evolutionary processes generated observed genomic patterns. Nonetheless, the studies in this section demonstrate ways forward toward bridging pattern and process, including experimental work, genetic mapping, increased knowledge of natural history and demography, and comparative studies spanning taxa at different points in the speciation continuum. Such collective work will lead to more powerful hypothesis testing. Future work can also help better integrate the contributions of ecology, genome structure (e.g., inversions and translocations), and genetic conflict to genome evolution., (© 2013 The Author(s). Evolution © 2013 The Society for the Study of Evolution.)

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., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

Diverse geographical modes and mechanisms of speciation are known, and individual speciation genes have now been identified. Despite this progress, genome-wide outcomes of different evolutionary processes during speciation are less understood. Here, we integrate ecological and spatial information, mating trials, transplantation data and analysis of 86 130 single nucleotide polymorphisms (SNPs) in eight populations (28 pairwise comparisons) of Timema cristinae stick insects to test the effects of different factors on genomic divergence in a system undergoing ecological speciation. We find patterns consistent with effects of numerous factors, including geographical distance, gene flow, divergence in host plant use and climate, and selection against maladaptive hybridization (i.e. reinforcement). For example, the number of highly differentiated 'outlier loci', allele-frequency clines and the overall distribution of genomic differentiation were recognizably affected by these factors. Although host use has strong effects on phenotypic divergence and reproductive isolation, its effects on genomic divergence were subtler and other factors had pronounced effects. The results demonstrate how genomic data can provide new insights into speciation and how genomic divergence can be complex, yet predictable. Future work could adopt experimental, mapping and functional approaches to directly test which genetic regions are affected by selection and determine their physical location in the genome.

The emerging field of speciation genomics is advancing our understanding of the evolution of reproductive isolation from the individual gene to a whole-genome perspective. In this new view it is important to understand the conditions under which 'divergence hitchhiking' associated with the physical linkage of gene regions, versus 'genome hitchhiking' associated with reductions in genome-wide rates of gene flow caused by selection, can enhance speciation-with-gene-flow. We describe here a theory predicting four phases of speciation, defined by changes in the relative effectiveness of divergence and genome hitchhiking, and review empirical data in light of the theory. We outline future directions, emphasizing the need to couple next-generation sequencing with selection, transplant, functional genomics, and mapping studies. This will permit a natural history of speciation genomics that will help to elucidate the factors responsible for population divergence and the roles that genome structure and different forms of hitchhiking play in facilitating the genesis of new biodiversity., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

Genetic differentiation during adaptive divergence and speciation is heterogeneous among genomic regions. Some regions can be highly differentiated between populations, for example, because they harbour genes under divergent selection or those causing reproductive isolation and thus are resistant to gene flow. Other regions might be homogenized by gene flow and thus weakly differentiated. Debates persist about the number of differentiated regions expected under divergence with gene flow, and their causes, size, and genomic distribution. In this issue of Molecular Ecology, a study of freshwater stickleback used next-generation sequencing to shed novel insight into these issues (Roesti et al. 2012). Many genomic regions distributed across the genome were strongly differentiated, indicating divergence with gene flow can involve a greater number of loci than often thought. Nonetheless, differentiation of some regions, such as those near the centre of chromosomes where recombination is reduced, was strongly accentuated over others. Thus, divergence was widespread yet highly heterogeneous across the genome. Moreover, different population pairs varied in patterns of differentiation, illustrating how genomic divergence builds up across stages of the speciation process. The study demonstrates how variation in different evolutionary processes, such as selection and recombination rate, can combine to result in similar genomic patterns. Future work could focus on teasing apart the contributions of different processes for causing differentiation, a task facilitated by experimental manipulations., (© 2012 Blackwell Publishing Ltd.)

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.

Theoretical models addressing genome-wide patterns of divergence during speciation are needed to help us understand the evolutionary processes generating empirical patterns. Here, we examine a critical issue concerning speciation-with-gene flow: to what degree does physical linkage (r < 0.5) of new mutations to already diverged genes aid the build-up of genomic islands of differentiation? We used simulation and analytical approaches to partition the probability of establishment for a new divergently selected mutation when the mutation (i) is the first to arise in an undifferentiated genome (the direct effect of selection), (ii) arises unlinked to any selected loci (r = 0.5), but within a genome that has some already diverged genes (the effect of genome-wide reductions in gene flow for facilitating divergence, which we term 'genome hitchhiking'), and (iii) arises in physical linkage to a diverged locus (divergence hitchhiking). We find that the strength of selection acting directly on a new mutation is generally the most important predictor for establishment, with divergence and genomic hitchhiking having smaller effects. We outline the specific conditions under which divergence and genome hitchhiking can aid mutation establishment. The results generate predictions about genome divergence at different points in the speciation process and avenues for further work.

Speciation with gene flow is greatly facilitated when traits subject to divergent selection also contribute to non-random mating. Such traits have been called 'magic traits', which could be interpreted to imply that they are rare, special, or unrealistic. Here, we question this assumption by illustrating that magic traits can be produced by a variety of mechanisms, including ones in which reproductive isolation arises as an automatic by-product of adaptive divergence. We also draw upon the theoretical literature to explore whether magic traits have a unique role in speciation or can be mimicked in their effects by physically linked trait-complexes. We conclude that magic traits are more frequent than previously perceived, but further work is needed to clarify their importance., (Copyright © 2011 Elsevier Ltd. All rights reserved.)

The long-standing goal of finding genes causing reproductive isolation is being achieved. To better link the genetics with the process of speciation, we propose that 'speciation gene' be defined as any gene contributing to the evolution of reproductive isolation. Characterizing a speciation gene involves establishing that the gene affects a component of reproductive isolation; demonstrating that divergence at the locus occurred before completion of speciation; and quantifying the effect size of the gene (i.e. the increase in total reproductive isolation caused by its divergence). Review of a sample of candidate speciation genes found that few meet these criteria. Improved characterization of speciation genes will clarify how numerous they are, their properties and how they affect genome-wide patterns of divergence.

Two models for speciation via selection have been proposed. In the well-known model of 'ecological speciation', divergent natural selection between environments drives the evolution of reproductive isolation. In a second 'mutation-order' model, different, incompatible mutations (alleles) fix in different populations adapting to the same selective pressure. How to demonstrate mutation-order speciation has been unclear, although it has been argued that it can be ruled out when gene flow occurs because the same, most advantageous allele will fix in all populations. However, quantitative examination of the interaction of factors influencing the likelihood of mutation-order speciation is lacking. We used simulation models to study how gene flow, hybrid incompatibility, selective advantage, timing of origination of new mutations and an initial period of allopatric differentiation affect population divergence via the mutation-order process. We find that at least some population divergence can occur under a reasonably wide range of conditions, even with moderate gene flow. However, strong divergence (e.g. fixation of different alleles in different populations) requires very low gene flow, and is promoted when (i) incompatible mutations have similar fitness advantages, (ii) less fit mutations arise slightly earlier in evolutionary time than more fit alternatives, and (iii) allopatric divergence occurs prior to secondary contact.

Ecological speciation is the process by which barriers to gene flow between populations evolve due to adaptive divergence via natural selection. A relatively unexplored area in ecological speciation is the role of gene expression. Gene expression may be associated with ecologically important phenotypes not evident from morphology and play a role during colonization of new environments. Here we review two potential roles of gene expression in ecological speciation: (1) its indirect role in facilitating population persistence and (2) its direct role in contributing to genetically based reproductive isolation. We find indirect evidence that gene expression facilitates population persistence, but direct tests are lacking. We also find clear examples of gene expression having effects on phenotypic traits and adaptive genetic divergence, but links to the evolution of reproductive isolation itself remain indirect. Gene expression during adaptive divergence seems to often involve complex genetic architectures controlled by gene networks, regulatory regions, and "eQTL hotspots." Nonetheless, we review how approaches for isolating the functional mutations contributing to adaptive divergence are proving to be successful. The study of gene expression has promise for increasing our understanding ecological speciation, particularly when integrative approaches are applied., (© 2010 New York Academy of Sciences.)

Genes under divergent selection flow less readily between populations than other loci. This observation has led to verbal "divergence hitchhiking" models of speciation in which decreased interpopulation gene flow surrounding loci under divergent selection can generate large regions of differentiation within the genome (genomic islands). The efficacy of this model in promoting speciation depends on the size of the region affected by divergence hitchhiking. Empirical evidence is mixed, with examples of both large and small genomic islands. To address these empirical discrepancies and to formalize the theory, we present mathematical models of divergence hitchhiking, which examine neutral differentiation around selected sites. For a single locus under selection, regions of differentiation do not extend far along a chromosome away from a selected site unless both effective population sizes and migration rates are low. When multiple loci are considered, regions of differentiation can be larger. However, with many loci under selection, genome-wide divergence occurs and genomic islands are erased. The results show that divergence hitchhiking can generate large regions of differentiation, but that the conditions under which this occurs are limited. Thus, speciation may often require multifarious selection acting on many, isolated and physically unlinked genes. How hitchhiking promotes further adaptive divergence warrants consideration.

Reinforcement, the evolution of prezygotic reproductive barriers by natural selection in response to maladaptive hybridization, is one of the most debated processes in speciation. Critics point to "fatal" conceptual flaws for sympatric evolution of prezygotic isolation, but recent theoretical and empirical work on genetics and ecology of reinforcement suggests that such criticisms can be overcome. New studies provide evidence for reinforcement in frogs, fish, insects, birds, and plants. While such evidence lays to rest the argument over reinforcement's existence, our understanding remains incomplete. We lack data on (1) the genetic basis of female preferences and the links between genetics of pre- and postzygotic isolation, (2) the ecological basis of reproductive isolation, (3) connections between prezygotic isolation between species and within-species sexual selection (potentially leading to a "cascade" of effects on reproductive isolation), (4) the role of habitat versus mate preference in reinforcement, and (5) additional detailed comparative studies. Here, we review data on these issues and highlight why they are important for understanding speciation.

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.

This study uses a comparative genome scan to evaluate the contributions of host plant related divergent selection to genetic differentiation and ecological speciation in maple- and willow-associated populations of Neochlamisus bebbianae leaf beetles. For each of 15 pairwise population comparisons, we identified "outlier loci" whose strong differentiation putatively reflects divergent selection. Of 447 AFLP loci, 15% were outliers across multiple population comparisons, and low linkage disequilibrium indicated that these outliers derived from multiple regions of the genome. Outliers were further classified as "host-specific" if repeatedly observed in "different-host" population comparisons but never in "same-host" comparisons. Outliers exhibiting the opposite pattern were analogously classified as "host-independent." Host-specific outliers represented 5% of all loci and were more frequent than host-independent outliers, thus revealing a large role for host-adaptation in population genomic differentiation. Evidence that host-related selection can promote divergence despite gene flow was provided by population trees. These were structured by host-association when datasets included host-specific outliers, but not when based on neutral loci, which united sympatric populations. Lastly, three host-specific outliers were highly differentiated in all nine different-host comparisons. Because host-adaptation promotes reproductive isolation in these beetles, these loci provide promising candidate gene regions for future molecular studies of ecological speciation.

The likelihood of speciation in the face of homogenizing gene flow (i.e. without complete geographical isolation) is one of the most debated topics in evolutionary biology. Demonstrating this phenonemon is hampered by the difficulty of isolating the effects of time since population divergence vs. gene flow on levels of molecular genetic differentiation. For example, weak genetic differentiation between taxa could be due to recent divergence, gene flow, or a combination of these factors. Nonetheless, a number of convincing examples of speciation with gene flow have recently emerged, owing in part to the development of new analytical methods designed to estimate gene flow specifically. A recent example of speciation with gene flow in salamanders (Niemiller et al. 2008) further advances our understanding of this phenonemon, by showing that gene flow between cave and spring salamanders was ongoing during speciation, rather than having occurred after a long period of allopatric divergence. Future work on the ecological and genetic factors reducing gene flow will likely increase our understanding of the conditions that faciliate divergence in the face of gene flow.

Sexual isolation can evolve due to natural selection against hybrids (reinforcement). However, many different forms of hybrid dysfunction, and selective processes that do not involve hybrids, can contribute to the evolution of sexual isolation. Here we review how different selective processes affect the evolution of sexual isolation, describe approaches for distinguishing among them, and assess how they contribute to variation in sexual isolation among populations of Timema cristinae stick-insects. Pairs of allopatric populations of T. cristinae living on different host-plant species exhibit greater sexual isolation than those on the same host, indicating that some sexual isolation has evolved due to host adaptation. Sexual isolation is strongest in regions where populations on different hosts are in geographic contact, a pattern of reproductive character displacement that is indicative of reinforcement. Ecological costs to hybridization do occur but traits under ecological selection (predation) do not co-vary strongly with the probability of between-population mating such that selection on ecological traits is not predicted to produce a strong correlated evolutionary response in mate preference. Moreover, F1 hybrid egg inviability is lacking and the factors contributing to reproductive character displacement require further study. Finally, we show that sexual isolation involves, at least in part, olfactory communication. Our results illustrate how understanding of the evolution of sexual isolation can be enhanced by isolating the roles of diverse ecological and evolutionary processes.

Speciation can involve the evolution of 'cryptic' reproductive isolation that occurs after copulation but before hybrid offspring are produced. Because such cryptic barriers to gene exchange involve post-mating sexual interactions, analyses of their evolution have focused on sexual conflict or traditional sexual selection. Here, we show that ecological divergence between populations of herbivorous walking sticks is integral to the evolution of cryptic reproductive isolation. Low female fitness following between-population mating can reduce gene exchange between populations, thus acting as a form of cryptic isolation. Female walking sticks show reduced oviposition rate and lower lifetime fecundity following between-population versus within-population mating, but only for mating between populations using different host-plant species. Our results indicate that even inherently sexual forms of reproductive isolation can evolve as a by-product of ecological divergence and that post-mating sexual interactions do not necessarily evolve independently of the ecological environment.

To what degree is the divergent adaptation responsible for life's phenotypic variety also responsible for generating the millions of species that manifest this variation? Theory predicts that ecological divergence among populations should promote reproductive isolation, and recent empirical studies provide support for this hypothesis in a limited number of specific taxa. However, the essential question of whether ecology plays a truly general role in speciation has yet to be systematically evaluated. Here we address this integral issue using an approach that adds an ecological dimension to comparative studies investigating the relationship between reproductive isolation and divergence time. Specifically, we quantify ecological divergence for >500 species pairs from eight plant, invertebrate, and vertebrate taxa and statistically isolate its association with reproductive isolation. This approach demonstrates a highly consistent and significant positive association between ecological divergence and reproductive isolation across taxa. This relationship was also observed across different aspects of ecological divergence and components of reproductive isolation. These findings are highly consistent with the hypothesis that ecological adaptation plays a fundamental and taxonomically general role in promoting reproductive isolation and speciation.

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. Speciation may not be a mechanistically or temporally uniform process. We show divergent evolution of sexual versus habitat isolation and flat versus linear accumulation of the latter for within- versus between-species comparisons, revealing a critical role for species. [ABSTRACT FROM AUTHOR]

Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC 27 Rundell RJ, Price TD. Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC 30 Feder JL, Berlocher SH, Roethele JB et al. Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC 18 Jombart T, Devillard S, Balloux F. BMC Genet 2010; 11: 94. 10.1186/1471-2156-11-94 Crossref Search ADS PubMed 19 Harrison RG. Speciation is not as mysterious as Darwin once described it [[1]]. [Extracted from the article]

Theory predicts that structural genomic variants such as inversions can promote adaptive diversification and speciation. Despite increasing empirical evidence that adaptive divergence can be triggered by one or a few large inversions, the degree to which widespread genomic regions under divergent selection are associated with structural variants remains unclear. Here we test for an association between structural variants and genomic regions that underlie parallel host‐plant‐associated ecotype formation in Timema cristinae stick insects. Using mate‐pair resequencing of 20 new whole genomes we find that moderately sized structural variants such as inversions, deletions and duplications are widespread across the genome, being retained as standing variation within and among populations. Using 160 previously published, standard‐orientation whole genome sequences we find little to no evidence that the DNA sequences within inversions exhibit accentuated differentiation between ecotypes. In contrast, a formerly described large region of reduced recombination that harbours genes controlling colour‐pattern exhibits evidence for accentuated differentiation between ecotypes, which is consistent with differences in the frequency of colour‐pattern morphs between host‐associated ecotypes. Our results suggest that some types of structural variants (e.g., large inversions) are more likely to underlie adaptive divergence than others, and that structural variants are not required for subtle yet genome‐wide genetic differentiation with gene flow. [ABSTRACT FROM AUTHOR]

Many hypotheses have been put forth to explain the origin and spread of inversions, and their significance for speciation. Several recent genic models have proposed that inversions promote speciation with gene flow due to the adaptive significance of the genes contained within them and because of the effects inversions have on suppressing recombination. However, the consequences of inversions for the dynamics of genome wide divergence across the speciation continuum remain unclear, an issue we examine here. We review a framework for the genomics of speciation involving the congealing of the genome into alternate adaptive states representing species ("genome wide congealing"). We then place inversions in this context as examples of how genetic hitchhiking can potentially hasten genome wide congealing. Specifically, we use simulation models to (i) examine the conditions under which inversions may speed genome congealing and (ii) quantify predicted magnitudes of these effects. Effects of inversions on promoting speciation were most common and pronounced when inversions were initially fixed between populations before secondary contact and adaptation involved many genes with small fitness effects. Further work is required on the role of underdominance and epistasis between a few loci of major effect within inversions. The results highlight five important aspects of the roles of inversions in speciation: (i) the geographic context of the origins and spread of inversions, (ii) the conditions under which inversions can facilitate divergence, (iii) the magnitude of that facilitation, (iv) the extent to which the buildup of divergence is likely to be biased within vs. outside of inversions, and (v) the dynamics of the appearance and disappearance of exceptional divergence within inversions. We conclude by discussing the empirical challenges in showing that inversions play a central role in facilitating speciation with gene flow. [ABSTRACT FROM AUTHOR]