PARALLEL EVOLUTION OF LOCAL ADAPTATION AND REPRODUCTIVE ISOLATION IN THE FACE OF GENE FLOW

Parallel evolution of similar phenotypes provides strong evidence for the operation of natural selection. Where these phenotypes contribute to reproductive isolation, they further support a role for divergent, habitat‐associated selection in speciation. However, the observation of pairs of divergent ecotypes currently occupying contrasting habitats in distinct geographical regions is not sufficient to infer parallel origins. Here we show striking parallel phenotypic divergence between populations of the rocky‐shore gastropod, Littorina saxatilis, occupying contrasting habitats exposed to either wave action or crab predation. This divergence is associated with barriers to gene exchange but, nevertheless, genetic variation is more strongly structured by geography than by ecotype. Using approximate Bayesian analysis of sequence data and amplified fragment length polymorphism markers, we show that the ecotypes are likely to have arisen in the face of continuous gene flow and that the demographic separation of ecotypes has occurred in parallel at both regional and local scales. Parameter estimates suggest a long delay between colonization of a locality and ecotype formation, perhaps because the postglacial spread of crab populations was slower than the spread of snails. Adaptive differentiation may not be fully genetically independent despite being demographically parallel. These results provide new insight into a major model of ecologically driven speciation.     

Divergent host-plant use promotes reproductive isolation among cynipid gall wasp populations

Ecological speciation occurs when reproductive isolation evolves as a consequence of divergent natural selection among environments. A direct prediction of this process is that ecologically divergent pairs of populations will exhibit greater reproductive isolation than ecologically similar pairs of populations. By comparing allopatric populations of the cynipid gall wasp Belonocnema treatae infesting Quercus virginiana and Quercus geminata, we tested the role that divergent host use plays in generating ecological divergence and sexual isolation. We found differences in body size and gall structure associated with divergent host use, but no difference in neutral genetic divergence between populations on the same or different host plant. We observed significant assortative mating between populations from alternative host plants but not between allopatric populations on the same host plant. Thus, we provide evidence that divergent host use promotes speciation among gall wasp populations.     

Divergence in coloration and ecological speciation in the Anolis marmoratus species complex

Adaptive divergence in coloration is expected to produce reproductive isolation in species that use colourful signals in mate choice and species recognition. Indeed, many adaptive radiations are characterized by differentiation in colourful signals, suggesting that divergent selection acting on coloration may be an important component of speciation. Populations in the Anolis marmoratus species complex from the Caribbean island of Guadeloupe display striking divergence in the colour and pattern of adult males that occurs over small geographic distances, suggesting strong divergent selection. Here we test the hypothesis that divergence in coloration results in reduced gene flow among populations. We quantify variation in adult male coloration across a habitat gradient between mesic and xeric habitats, use a multilocus coalescent approach to infer historical demographic parameters of divergence, and examine gene flow and population structure using microsatellite variation. We find that colour variation evolved without geographic isolation and in the face of gene flow, consistent with strong divergent selection and that both ecological and sexual selection are implicated. However, we find no significant differentiation at microsatellite loci across populations, suggesting little reproductive isolation and high levels of contemporary gene exchange. Strong divergent selection on loci affecting coloration probably maintains clinal phenotypic variation despite high gene flow at neutral loci, supporting the notion of a porous genome in which adaptive portions of the genome remain fixed whereas neutral portions are homogenized by gene flow and recombination. We discuss the impact of these findings for studies of colour evolution and ecological speciation.     

ADAPTIVE POPULATION DIVERGENCE IN CRYPTIC COLOR-PATTERN FOLLOWING A REDUCTION IN GENE FLOW

Adaptive population divergence is often driven by divergent natural selection, but can be constrained by the homogenizing effect of gene flow between populations. Indeed, a common pattern in nature is an inverse correlation between the degree of adaptive phenotypic divergence between populations and levels of gene flow between populations. However, there is essentially no experimental data on whether this correlation arises because gene flow constrains adaptation or, conversely, because adaptive divergence causes barriers to gene flow (ecological speciation). Here, I report increased adaptive divergence in cryptic color pattern between a pair of Timema insect populations following an experimental reduction in between-population gene flow. The reduction in gene flow arose due to a natural experiment, and thus was not replicated at a second site. However, temporal replication of the trends among six generations of data, coupled with a lack of increased adaptive divergence for two other population pairs where gene flow was not manipulated (i.e., control sites), argues that the results did not arise by chance. Estimates of dispersal ability and population size further support reduced gene flow, rather than increased genetic drift, as the cause of divergence. Thus, the findings provide experimental evidence that gene flow constrains adaptation in nature.     

Ernst Mayr and the integration of geographic and ecological factors in speciation

Mayr's best recognized scientific contributions include the biological species concept and the theory of geographic speciation. In the latter, reproductive isolation evolves as an incidental by‐product of genetic divergence between allopatric populations. Mayr noted that divergent natural selection could accelerate speciation, but also argued that gene flow so strongly retards divergence that, even with selection, non‐allopatric speciation is unlikely. However, current theory and data demonstrate that substantial divergence, and even speciation, in the face of gene flow is possible. Here, I attempt to connect some opposing views about speciation by integrating Mayr's ideas about the roles of ecology and geography in speciation with current data and theory. My central premise is that the speciation process (i.e. divergence) is often continuous, and that the opposing processes of selection and gene flow interact to determine the degree of divergence (i.e. the degree of progress towards the completion of speciation). I first establish that, in the absence of gene flow, divergent selection often promotes speciation. I then discuss how population differentiation in the face of gene flow is common when divergent selection occurs. However, such population differentiation does not always lead to the evolution of discontinuities, strong reproductive isolation, and thus speciation per se. I therefore explore the genetic and ecological circumstances that facilitate speciation in the face of gene flow. For example, particular genetic architectures or ecological niches may tip the balance between selection and gene flow strongly in favour of selection. The circumstances allowing selection to overcome gene flow to the extent that a discontinuity develops, and how often these circumstances occur, are major remaining questions in speciation research. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 26–46.     

Local adaptation within a hybrid species

Ecological divergence among populations may be strongly influenced by their genetic background. For instance, genetic admixture through introgressive hybridization or hybrid speciation is likely to affect the genetic variation and evolvability of phenotypic traits. We studied geographic variation in two beak dimensions and three other phenotypic traits of the Italian sparrow (Passer italiae), a young hybrid species formed through interbreeding between house sparrows (P. domesticus) and Spanish sparrows (P. hispaniolensis). We found that beak morphology was strongly influenced by precipitation regimes and that it appeared to be the target of divergent selection within Italian sparrows. Interestingly, however, the degree of parental genetic contribution in the hybrid species had no effect on phenotypic beak variation. Moreover, beak height divergence may mediate genetic differentiation between populations, consistent with isolation-by-adaptation within this hybrid species. The study illustrates how hybrid species may be relatively unconstrained by their admixed genetic background, allowing them to adapt rapidly to environmental variation.     

The evolution of host preference in allopatric vs. parapatric populations of Timema cristinae walking-sticks

Divergent habitat preferences can contribute to speciation, as has been observed for host-plant preferences in phytophagous insects. Geographic variation in host preference can provide insight into the causes of preference evolution. For example, selection against maladaptive host-switching occurs only when multiple hosts are available in the local environment and can result in greater divergence in regions with multiple vs. a single host. Conversely, costs of finding a suitable host can select for preference even in populations using a single host. Some populations of Timema cristinae occur in regions with only one host-plant species present (in allopatry, surrounded by unsuitable hosts) whereas others occur in regions with two host-plant species adjacent to one another (in parapatry). Here, we use host choice and reciprocal-rearing experiments to document genetic divergence in host preference among 33 populations of T. cristinae. Populations feeding on Ceanothus exhibited a stronger preference for Ceanothus than did populations feeding on Adenostoma. Both allopatric and parapatric pairs of populations using the different hosts exhibited divergent host preferences, but the degree of divergence tended to be greater between allopatric pairs. Thus, gene flow between parapatric populations apparently constrains divergence. Host preferences led to levels of premating isolation between populations using alternate hosts that were comparable in magnitude to previously documented premating isolation caused by natural and sexual selection against migrants between hosts. Our findings demonstrate how gene flow and different forms of selection interact to determine the magnitude of reproductive isolation observed in nature.     

Diversification across a heterogeneous landscape

Adaptation to contrasting environments across a heterogeneous landscape favors the formation of ecotypes by promoting ecological divergence. Patterns of fitness variation in the field can show whether natural selection drives local adaptation and ecotype formation. However, to demonstrate a link between ecological divergence and speciation, local adaptation must have consequences for reproductive isolation. Using contrasting ecotypes of an Australian wildflower, Senecio lautus in common garden experiments, hybridization experiments, and reciprocal transplants, we assessed how the environment shapes patterns of adaptation and the consequences of adaptive divergence for reproductive isolation. Local adaptation was strong between ecotypes, but weaker between populations of the same ecotype. F1 hybrids exhibited heterosis, but crosses involving one native parent performed better than those with two foreign parents. In a common garden experiment, F2 hybrids exhibited reduced fitness compared to parentals and F1 hybrids, suggesting that few genetic incompatibilities have accumulated between populations adapted to contrasting environments. Our results show how ecological differences across the landscape have created complex patterns of local adaptation and reproductive isolation, suggesting that divergent natural selection has played a fundamental role in the early stages of species diversification.     

Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks

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.     

DISENTANGLING THE ROLE OF PHENOTYPIC PLASTICITY AND GENETIC DIVERGENCE IN CONTEMPORARY ECOTYPE FORMATION DURING A BIOLOGICAL INVASION

The occurrence of contemporary ecotype formation through adaptive divergence of populations within the range of an invasive species typically requires standing genetic variation but can be facilitated by phenotypic plasticity. The relative contributions of both of these to adaptive trait differentiation have rarely been simultaneously quantified in recently diverging vertebrate populations. Here we study a case of intraspecific divergence into distinct lake and stream ecotypes of threespine stickleback that evolved in the past 140 years within the invasive range in Switzerland. Using a controlled laboratory experiment with full‐sib crosses and treatments mimicking a key feature of ecotypic niche divergence, we test if the phenotypic divergence that we observe in the wild results from phenotypic plasticity or divergent genetic predisposition. Our experimental groups show qualitatively similar phenotypic divergence as those observed among wild adults. The relative contribution of plasticity and divergent genetic predisposition differs among the traits studied, with traits related to the biomechanics of feeding showing a stronger genetic predisposition, whereas traits related to locomotion are mainly plastic. These results implicate that phenotypic plasticity and standing genetic variation interacted during contemporary ecotype formation in this case.     

Divergence and reproductive isolation in the early stages of speciation

To understand speciation we need to identify the factors causing divergence between natural populations. The traditional approach to gaining such insights has been to focus on a particular theory and ask whether observed patterns of reproductive isolation between populations or species are consistent with the hypothesis in question. However, such studies are few and they do not allow us to compare between hypotheses, so often we cannot determine the relative contribution to divergence of different potential factors. Here, I describe a study of patterns of phenotypic divergence and premating and postmating isolation between populations of the grasshopper Chorthippus parallelus. Information on the phylogeographic relationships of the populations means that a priori predictions from existing hypotheses for the evolution of reproductive isolation can be compared with observations. I assess the relative contributions to premating isolation, postmating isolation and phenotypic divergence of long periods of allopatry, adaptation to different environments and processes associated with colonisation (such as population bottlenecks). Likelihood analysis reveals that long periods of allopatry in glacial refugia are associated with postmating reproductive isolation, but not premating isolation, which is more strongly associated with colonisation. Neither premating nor postmating isolation is higher between populations differing in potential environmental selection pressures. There are only weak correlations between patterns of genetic divergence and phenotypic divergence and no correlation between premating and postmating isolation. This suggests that the potential of a taxon to exercise mate choice may affect the types of factor that promote speciation in that group. I discuss the advantages and disadvantages of the general approach of simultaneously testing competing hypotheses for the evolution of reproductive isolation.     

生态物种形成及其研究进展

物种形成是基本的进化过程, 也是生物多样性形成的基础。自然选择可以导致新物种的产生。生态物种形成是指以生态为基础的歧化选择使不同群体分化产生生殖隔离的物种形成过程。本文首先回顾了生态物种形成的研究历史, 并详细介绍了生态物种形成的3个要素, 即歧化选择的来源、生殖隔离的形式以及关联歧化选择与生殖隔离的遗传机制。歧化选择的来源主要包括不同的环境或生态位、不同形式的性选择, 以及群体间的相互作用。生殖隔离的形式多种多样, 我们总结了合子前和合子后隔离的遗传学机制以及在生态物种形成中起到的作用。控制适应性性状的基因与导致生殖隔离的基因可以通过基因多效性或连锁不平衡相互关联起来。借助于第二代测序技术, 研究者可以对生态物种形成的遗传学与基因组学基础进行研究。此外, 本文还总结了生态物种形成领域最新的研究进展, 包括平行进化的全基因组基础, 以及基因流影响群体分化的理论基础。通过归纳比较由下至上和由上至下这两种不同的研究思路, 作者认为这两种思路的结合可以为生态物种形成基因的筛选提供更有力也更精确的方法。同时, 作者还提出生态物种形成的研究应该基于更好的表型描述以及更完整的基因组信息, 研究的物种也应该具有更广泛的代表性。     

Testing the role of climate in speciation: New methods and applications to squamate reptiles (lizards and snakes)

Climate may play important roles in speciation, such as causing the range fragmentation that underlies allopatric speciation (through niche conservatism) or driving divergence of parapatric populations along climatic gradients (through niche divergence). Here, we developed new methods to test the frequency of climate niche conservatism and divergence in speciation, and applied it to species pairs of squamate reptiles (lizards and snakes). We used a large‐scale phylogeny to identify 242 sister species pairs for analysis. From these, we selected all terrestrial allopatric pairs with sufficient occurrence records (n = 49 pairs) and inferred whether each originated via climatic niche conservatism or climatic niche divergence. Among the 242 pairs, allopatric pairs were most common (41.3%), rather than parapatric (19.4%), partially sympatric (17.7%), or fully sympatric species pairs (21.5%). Among the 49 selected allopatric pairs, most appeared to have originated via climatic niche divergence (61–76%, depending on the details of the methods). Surprisingly, we found greater climatic niche divergence between allopatric sister species than between parapatric pairs, even after correcting for geographic distance. We also found that niche divergence did not increase with time, further implicating niche divergence in driving lineage splitting. Overall, our results suggest that climatic niche divergence may often play an important role in allopatric speciation, and the methodology developed here can be used to address the generality of these findings in other organisms.     

Low reproductive isolation and highly variable levels of gene flow reveal limited progress towards speciation between European river and brook lampreys

Ecologically based divergent selection is a factor that could drive reproductive isolation even in the presence of gene flow. Population pairs arrayed along a continuum of divergence provide a good opportunity to address this issue. Here, we used a combination of mating trials, experimental crosses and population genetic analyses to investigate the evolution of reproductive isolation between two closely related species of lampreys with distinct life histories. We used microsatellite markers to genotype over 1000 individuals of the migratory parasitic river lamprey (Lampetra fluviatilis) and freshwater‐resident nonparasitic brook lamprey (Lampetra planeri) distributed in 10 sympatric and parapatric population pairs in France. Mating trials, parentage analyses and artificial fertilizations demonstrated a low level of reproductive isolation between species even though size‐assortative mating may contribute to isolation. Most parapatric population pairs were strongly differentiated due to the joint effects of geographic distance and barriers to migration. In contrast, we found variable levels of gene flow between sympatric populations ranging from panmixia to moderate differentiation, which indicates a gradient of divergence with some population pairs that may correspond to alternative morphs or ecotypes of a single species and others that remain partially isolated. Ecologically based divergent selection may explain these variable levels of divergence among sympatric population pairs, but incomplete genome swamping following secondary contact could have also played a role. Overall, this study illustrates how highly differentiated phenotypes can be maintained despite high levels of gene flow that limit the progress towards speciation.     

Do highly divergent loci reside in genomic regions affecting reproductive isolation? A test using next-generation sequence data in Timema stick insects

ABSTRACT: BACKGROUND: Genetic divergence during speciation with gene flow is heterogeneous across the genome, with some regions exhibiting stronger differentiation than others. Exceptionally differentiated regions are often assumed to experience reduced introgression, i.e., reduced flow of alleles from one population into another because such regions are affected by divergent selection or cause reproductive isolation. In contrast, the remainder of the genome can be homogenized by high introgression. Although many studies have documented variation across the genome in genetic differentiation, there are few tests of this hypothesis that explicitly quantify introgression. Here, we provide such a test using 38,304 SNPs in populations of Timema cristinae stick insects. We quantify whether loci that are highly divergent between geographically separated ('allopatric') populations exhibit unusual patterns of introgression in admixed populations. To the extent this is true, highly divergent loci between allopatric populations contribute to reproductive isolation in admixed populations. RESULTS: As predicted, we find a substantial association between locus-specific divergence between allopatric populations and locus-specific introgression in admixed populations. However, many loci depart from this relationship, sometimes strongly so. We also report evidence for selection against foreign alleles due to local adaptation. CONCLUSIONS: Loci that are strongly differentiated between allopatric populations sometimes contribute to reproductive isolation in admixed populations. However, geographic variation in selection and local adaptation, in aspects of genetic architecture (such as organization of genes, recombination rate variation, number and effect size of variants contributing to adaptation, etc.), and in stochastic evolutionary processes such as drift can cause strong differentiation of loci that do not always contribute to reproductive isolation. The results have implications for the theory of 'genomic islands of speciation'.     

Refugial isolation versus ecological gradients

Hypotheses for divergence and speciation in rainforests generally fall into two categories: those emphasizing the role of geographic isolation and those emphasizing the role of divergent selection along gradients. While a majority of studies have attempted to infer mechanisms based on the pattern of species richness and congruence of geographic boundaries, relatively few have tried to simultaneously test alternative hypotheses for diversification. Here we discuss four examples, taken from our work on diversification of tropical rainforest vertebrates, in which we examine patterns of genetic and morphological variation within and between biogeographic regions to address two alternative hypotheses. By estimating morphological divergence between geographically contiguous and isolated populations under similar and different ecological conditions, we attempt to evaluate the relative roles of geographic isolation and natural selection in population divergence. Results suggest that natural selection, even in the presence of appreciable gene flow, can result in morphological divergence that is greater than that found between populations isolated for millions of years and, in some cases, even greater than that found between congeneric, but distinct, species. The relatively small phenotypic divergence that occurs among long-term geographic isolates in similar habitats suggests that morphological divergence via drift may be negligible and/or that selection is acting to produce similar phenotypes in populations occupying similar habitats. Our results demonstrate that significant phenotypic divergence: (1) is not necessarily coupled with divergence in neutral molecular markers; and (2) can occur without geographic isolation in the presence of gene flow.     

Coevolution of male mating signal and female preference during early lineage divergence of the Hawaiian cricket, Laupala cerasina

Sexual selection is a powerful evolutionary force shaping mate choice phenotypes, initiating phenotypic shifts resulting in (or reinforcing) population divergence and speciation when such shifts reduce mating probabilities among divergent populations. In the Hawaiian cricket genus Laupala, pulse rate of male calling song, a conspicuous mating signal, differs among species, potentially behaving as a speciation phenotype. Populations of the widespread species Laupala cerasina show variation in pulse rate. We document the degree of population differentiation in three features of calling song: pulse rate, pulse duration, and carrier frequency. All show significant population differentiation, with pulse rate showing the greatest heterogeneity. A Mantel test found no relationship between geographic distance and pulse rate divergence, indicating that a simple model of greater divergence with increasing distance cannot explain the observed pattern of differentiation. We demonstrate that female preference functions for pulse rate are unimodal, and that preference means show significant differentiation among populations. Furthermore, estimates of pulse rate preference correlate significantly with mean pulse rates across populations, indicating song and preference coevolve in a stepwise manner. This correlated divergence between signal and preference suggests that sexual selection facilitates the establishment of sexual isolation, reduced gene flow, and population differentiation, prerequisites for speciation.     

Genome-wide patterns of divergence during speciation: the lake whitefish case study

The nature, size and distribution of the genomic regions underlying divergence and promoting reproductive isolation remain largely unknown. Here, we summarize ongoing efforts using young (12 000 yr BP) species pairs of lake whitefish (Coregonus clupeaformis) to expand our understanding of the initial genomic patterns of divergence observed during speciation. Our results confirmed the predictions that: (i) on average, phenotypic quantitative trait loci (pQTL) show higher F(ST) values and are more likely to be outliers (and therefore candidates for being targets of divergent selection) than non-pQTL markers; (ii) large islands of divergence rather than small independent regions under selection characterize the early stages of adaptive divergence of lake whitefish; and (iii) there is a general trend towards an increase in terms of numbers and size of genomic regions of divergence from the least (East L.) to the most differentiated species pair (Cliff L.). This is consistent with previous estimates of reproductive isolation between these species pairs being driven by the same selective forces responsible for environment specialization. Altogether, dwarf and normal whitefish species pairs represent a continuum of both morphological and genomic differentiation contributing to ecological speciation. Admittedly, much progress is still required to more finely map and circumscribe genomic islands of speciation. This will be achieved through the use of next generation sequencing data but also through a better quantification of phenotypic traits moulded by selection as organisms adapt to new environmental conditions.     

Interspecific Competition and Speciation in Endoparasitoids

Ecological speciation occurs when inherent reproductive barriers to gene flow evolve between populations as a result of divergent natural selection. Frequency dependent effects associated with intraspecific resource competition are thought to be one important source of divergent selection facilitating ecological speciation. Interspecific competition may also play an important role in promoting population divergence. Although evidence for interspecific competition in nature is ubiquitous, there is currently little empirical data supporting its role in the speciation process. Here, we discuss two general models in which interspecific competition among species can promote ecological speciation among populations within a species. In both models, interspecific competition is the source of divergent selection driving adaption to different portions of the resource distribution, generating ecological reproductive isolation from other conspecific populations. We propose that the biology of endoparasitoids that attack phytophagous insects make model systems for studying the role of interspecific competition in ecological speciation. We describe details for one such system, the community of endoparasitic braconid wasps attacking Rhagoletis fruit flies, as a potential model for investigating competitive speciation. We conclude by hypothesizing that a model in which interspecific competition forces an inferior competitor to alternative fly hosts may be a common theme contributing to parasitoid diversification in the Rhagoletis-parasitoid system.