Sculpin hybrid zones: natural laboratories for the early stages of speciation

Firmly rooted as we are in the genomic era, it can seem incredible that as recently as 1974, Lewontin declared, 'we know virtually nothing about the genetic changes that occur in species formation'. To the contrary, we now know the genetic architecture of phenotypic differences and reproductive isolation between species for many diverse groups of plants, animals, and fungi. In recent years, detailed genetic analyses have produced a small but growing list of genes that cause reproductive isolation, several of which appear to have diverged by natural selection. Yet, a full accounting of the speciation process requires that we understand the reproductive and ecological properties of natural populations as they begin to diverge genetically, as well as the dynamics of newly evolved barriers to gene flow. One promising approach to this problem is the study of natural hybrid zones, where gene exchange between divergent populations can produce recombinant genotypes in situ . In such individuals, genomic variation might be shaped by introgression at universally adaptive or neutral loci, even as regions associated with local adaptation or reproductive isolation remain divergent. In Nolte et   al . (2009) , the authors take advantage of two independent, recently formed hybrid zones between sculpin species to investigate genome-wide patterns of reproductive isolation. Using a recently developed genomic clines method, the authors identify marker loci that are associated with isolation, and those that show evidence for adaptive introgression. Remarkably, Nolte et   al . (2009) find little similarity between the two hybrid zones in patterns of introgression, a fact that might reflect genetic variation within species or heterogeneous natural selection. In either case, their study system has the potential to provide insight into the early stages of speciation.     

Recombination and the divergence of hybridizing species

The interplay between hybridization and recombination can have a dramatic effect on the likelihood of speciation or persistence of incompletely isolated species. Many models have suggested recombination can oppose speciation, and several recent empirical investigations suggest that reductions in recombination between various components of reproductive isolation and/or adaptation can allow species to persist in the presence of gene flow. In this article, we discuss these ideas in relation to speciation models, phylogenetic analyses, and species concepts. In particular, we revisit genetic architectures and population mechanisms that create genetic correlations and facilitate divergence in the face of gene flow. Linkage among genes contributing to adaptation or reproductive isolation due to chromosomal rearrangements as well as pleiotropy or proximity of loci can greatly increase the odds of species divergence or persistence. Finally, we recommend recombination to be a focus of inquiry when studying the origins of biological diversity.     

Patterns of parapatric speciation

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

THE BIOLOGY OF SPECIATION

Since Darwin published the “Origin,” great progress has been made in our understanding of speciation mechanisms. The early investigations by Mayr and Dobzhansky linked Darwin's view of speciation by adaptive divergence to the evolution of reproductive isolation, and thus provided a framework for studying the origin of species. However, major controversies and questions remain, including: When is speciation nonecological? Under what conditions does geographic isolation constitute a reproductive isolating barrier? and How do we estimate the “importance” of different isolating barriers? Here, we address these questions, providing historical background and offering some new perspectives. A topic of great recent interest is the role of ecology in speciation. “Ecological speciation” is defined as the case in which divergent selection leads to reproductive isolation, with speciation under uniform selection, polyploid speciation, and speciation by genetic drift defined as “nonecological.” We review these proposed cases of nonecological speciation and conclude that speciation by uniform selection and polyploidy normally involve ecological processes. Furthermore, because selection can impart reproductive isolation both directly through traits under selection and indirectly through pleiotropy and linkage, it is much more effective in producing isolation than genetic drift. We thus argue that natural selection is a ubiquitous part of speciation, and given the many ways in which stochastic and deterministic factors may interact during divergence, we question whether the ecological speciation concept is useful. We also suggest that geographic isolation caused by adaptation to different habitats plays a major, and largely neglected, role in speciation. We thus provide a framework for incorporating geographic isolation into the biological species concept (BSC) by separating ecological from historical processes that govern species distributions, allowing for an estimate of geographic isolation based upon genetic differences between taxa. Finally, we suggest that the individual and relative contributions of all potential barriers be estimated for species pairs that have recently achieved species status under the criteria of the BSC. Only in this way will it be possible to distinguish those barriers that have actually contributed to speciation from those that have accumulated after speciation is complete. We conclude that ecological adaptation is the major driver of reproductive isolation, and that the term “biology of speciation,” as proposed by Mayr, remains an accurate and useful characterization of the diversity of speciation mechanisms.     

Variation in reproductive isolation across a species range

Reproductive isolation is often variable within species, a phenomenon that while largely ignored by speciation studies, can be leveraged to gain insight into the potential mechanisms driving the evolution of genetic incompatibilities. We used experimental greenhouse crosses to characterize patterns of reproductive isolation among three divergent genetic lineages of Campanulastrum americanum that occur in close geographic proximity in the Appalachian Mountains. Substantial, asymmetrical reproductive isolation for survival due to cytonuclear incompatibility was found among the lineages (up to 94% reduction). Moderate reductions in pollen viability, as well as cytoplasmic male sterility, were also found between some Mountain populations. We then compared these results to previously established patterns of reproductive isolation between these Mountain lineages and a fourth, widespread Western lineage to fully characterize reproductive isolation across the complete geographic and genetic range of C. americanum. Reproductive isolation for survival and pollen viability was consistent across studies, indicating the evolution of the underlying genetic incompatibilities is primarily determined by intrinsic factors. In contrast, reproductive isolation for germination was only found when crossing Mountain populations with the Western lineage, suggesting the underlying genetic incompatibility is likely influenced by environmental or demographic differences between the two lineages. Cytoplasmic male sterility was also limited in occurrence, being restricted to a handful of Mountain populations in a narrow geographic range. These findings illustrate the complexity of speciation by demonstrating multiple, independent genetic incompatibilities that lead to a mosaic of genetic divergence and reproductive isolation across a species range.     

Ecogeographic isolation: a reproductive barrier between species and between cytotypes in Houstonia (Rubiaceae)

‘Ecogeographic isolation’ describes the combined role of ecology and geography as a reproductive barrier, and an important component in speciation. Evidence increasingly shows that this form of isolation is important for maintaining the genetic integrity of populations and species. Further, ecogeographic isolation can be a reproductive barrier between polyploid individuals and their diploid progenitors. New ecoinformatic methods, which includes niche modeling and associated statistical assessments of these models with spatially explicit environmental data, allow us to test if ecogeographic isolation is a contributing isolating barrier between species and between cytotypes within a species. We tested the hypothesis that ecogeographic isolation contributes to isolation of species and cytotypes within species of the plant genus Houstonia. We found that species in this group occupied significantly different niches, which suggests ecogeographic isolation is a contributing reproductive barrier. We also found that diploid and tetraploid forms of H. longifolia show some level of ecogeographic isolation, but H. purpurea diploids and tetraploids did not. Our results suggest that ecogeographic isolation plays a role in reproductive isolation between Houstonia species and between cytotypes of H. longifolia.     

A guide to the genomics of ecological speciation in natural animal populations

Interest in ecological speciation is growing, as evidence accumulates showing that natural selection can lead to rapid divergence between subpopulations. However, whether and how ecological divergence can lead to the buildup of reproductive isolation remains under debate. What is the relative importance of natural selection vs. neutral processes? How does adaptation generate reproductive isolation? Can ecological speciation occur despite homogenizing gene flow? These questions can be addressed using genomic approaches, and with the rapid development of genomic technology, will become more answerable in studies of wild populations than ever before. In this article, we identify open questions in ecological speciation theory and suggest useful genomic methods for addressing these questions in natural animal populations. We aim to provide a practical guide for ecologists interested in incorporating genomic methods into their research programs. An increased integration between ecological research and genomics has the potential to shed novel light on the origin of species.     

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.     

Natural selection reinforces speciation in a radiation of neotropical rainforest plants

The importance of reinforcement, that is, natural selection that strengthens reproductive isolation between incipient species, remains controversial. We used two approaches to test for reinforcement in a species radiation of Neotropical gingers in the genus Costus. First, we conducted an intensive study of Costus pulverulentus and Costus scaber, two recently diverged species that co-occur and share hummingbird pollinators. The hummingbird pollinators transfer pollen between these Costus species, but hybrids are rarely found in nature. By performing pollinations between populations of C. pulverulentus and C. scaber from three sites across the species' geographic ranges, we find that pollen-pistil incompatibilities acting prior to fertilization have evolved only between locally sympatric populations, whereas geographically distant populations within the region of sympatry and allopatric populations remain fully interfertile. Second, we conducted a comparative study of isolating mechanisms across the genus. We find lower seed set due to pollen-pistil incompatibility between species pairs that co-occur and experience pollen transfer in nature compared to species pairs that are otherwise isolated, regardless of genetic distance. Taken together, these studies indicate that crossing barriers prevent potentially maladaptive hybridization and effectively reinforce the speciation process. Our results add to mounting evidence for reinforcement from animal studies and show that plant speciation may also involve complex mate recognition systems. Reinforcement may be particularly important in rapidly diverging lineages where ecological factors play a primary role in reproductive isolation, as may often be the case in tropical communities.     

Chromosomal variation segregates within incipient species and correlates with reproductive isolation

Reproductive isolation is a critical step in the process of speciation. Among the most important factors driving reproductive isolation are genetic incompatibilities. Whether these incompatibilities are already present before extrinsic factors prevent gene flow between incipient species remains largely unresolved in natural systems. This question is particularly challenging because it requires that we catch speciating populations in the act before they reach the full‐fledged species status. We measured the extent of intrinsic postzygotic isolation within and between phenotypically and genetically divergent lineages of the wild yeast Saccharomyces paradoxus that have partially overlapping geographical distributions. We find that hybrid viability between lineages progressively decreases with genetic divergence. A large proportion of postzygotic inviability within lineages is associated with chromosomal rearrangements, suggesting that chromosomal differences substantially contribute to the early steps of reproductive isolation within lineages before reaching fixation. Our observations show that polymorphic intrinsic factors may segregate within incipient species before they contribute to their full reproductive isolation and highlight the role of chromosomal rearrangements in speciation. We propose different hypotheses based on adaptation, biogeographical events and life history evolution that could explain these observations.     

Natural and sexual selection against immigrants maintains differentiation among micro‐allopatric populations

Local adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and hence lead to speciation. But what mechanisms contribute to reproductive isolation among diverging populations? We tested for natural and sexual selection against immigrants in a fish species inhabiting (and adapting to) nonsulphidic surface habitats, sulphidic surface habitats and a sulphidic cave. Gene flow is strong among sample sites situated within the same habitat type, but low among divergent habitat types. Our results indicate that females of both sulphidic populations discriminate against immigrant males during mate choice. Furthermore, using reciprocal translocation experiments, we document natural selection against migrants between nonsulphidic and sulphidic habitats, whereas migrants between sulphidic cave and surface habitats did not exhibit increased mortality within the same time period. Consequently, both natural and sexual selection may contribute to isolation among parapatric populations, and selection against immigrants may be a powerful mechanism facilitating speciation among locally adapted populations even over very small spatial distances.     

Why do species exist? Insights from sexuals and asexuals

Why does life diversify into the more or less discrete entities we recognise as species? Two main explanations have been proposed: i) species are a consequence of adaptation to different ecological niches, ii) species are a consequence of sexual reproduction and reproductive isolation. Phylogenetic studies of case-study groups can provide insights into the relative importance of divergent selection and isolation for speciation, but it can be difficult to infer causes of speciation unambiguously. The example of North American tiger beetles from the genus Cicindela is discussed. An alternative approach is to compare diversification between related sexual and asexual taxa to infer the relative importance of the two explanations. We outline expected patterns of diversification in sexual and asexual lineages under different scenarios using coalescent theory. Whether sexuals or asexuals diversify to a greater extent depends on the balance among various stages of diversification, particularly on the effects of sexual reproduction on rates of adaptive evolution. Rotifers offer a unique system to test these ideas, allowing comparison of patterns of genetic and functional morphological diversification in sexual (bdelloid) and asexual (monogonont) clades.     

Thermal adaptation and ecological speciation

Ecological speciation is defined as the emergence of reproductive isolation as a direct or indirect consequence of divergent ecological adaptation. Several empirical examples of ecological speciation have been reported in the literature which very often involve adaptation to biotic resources. In this review, we investigate whether adaptation to different thermal habitats could also promote speciation and try to assess the importance of such processes in nature. Our survey of the literature identified 16 animal and plant systems where divergent thermal adaptation may underlie (partial) reproductive isolation between populations or may allow the stable coexistence of sibling taxa. In many of the systems, the differentially adapted populations have a parapatric distribution along an environmental gradient. Isolation often involves extrinsic selection against locally maladapted parental or hybrid genotypes, and additional pre- or postzygotic barriers may be important. Together, the identified examples strongly suggest that divergent selection between thermal environments is often strong enough to maintain a bimodal genotype distribution upon secondary contact. What is less clear from the available data is whether it can also be strong enough to allow ecological speciation in the face of gene flow through reinforcement-like processes. It is possible that intrinsic features of thermal gradients or the genetic basis of thermal adaptation make such reinforcement-like processes unlikely but it is equally possible that pertinent systems are understudied. Overall, our literature survey highlights (once again) the dearth of studies that investigate similar incipient species along the continuum from initial divergence to full reproductive isolation and studies that investigate all possible reproductive barriers in a given system.     

Divergent strategies in pre‐ and postzygotic reproductive isolation between two closely related Dianthus species

Quantifying the relative contribution of multiple isolation barriers to gene flow between recently diverged species is essential for understanding speciation processes. In parapatric populations, local adaptation is thought to be a major contributor to the evolution of reproductive isolation. However, extrinsic postzygotic barriers assessed in reciprocal transplant experiments are often neglected in empirical assessments of multiple isolation barriers. We analyzed multiple isolation barriers between two closely related species of the plant genus Dianthus, a genus characterized by the most rapid species diversification in plants reported so far. Although D. carthusianorum L. and D. sylvestris Wulf. can easily be hybridized in crossing experiments, natural hybrids are rare. We found that in parapatry, pollinator‐mediated prezygotic reproductive isolation barriers are important for both D. carthusianorum (0.761) and D. sylvestris (0.468). In contrast to D. carthusianorum, high hybrid viability in D. sylvestris (–0.491) was counteracted by strong extrinsic postzygotic isolation (0.900). Our study highlights the importance of including reciprocal transplant experiments for documenting extrinsic postzygotic isolation and demonstrates clearly divergent strategies and hence asymmetric pre‐ and postzygotic reproductive isolation between closely related species. It also suggests that pollinator‐mediated and ecological isolation could have interacted in synergistic ways, further stimulating rapid speciation in Dianthus.     

Disassociation between weak sexual isolation and genetic divergence in a hermaphroditic land snail and implications about chirality

Examination of the association between reproductive isolation and genetic divergence in a variety of organisms is essential for elucidating the mechanisms causing speciation. However, such studies are lacking for hermaphrodites. We measured premating (sexual) isolation in species pairs of the hermaphroditic land snail Albinaria and we compared it with their genetic divergence. We did not find substantial sexual isolation barriers between the species studied. The absence of strong sexual isolation between species implies its minor effect in the evolution of this genus, because distributional, population and life-history characteristics of Albinaria make mate-choice possibly redundant. Furthermore, we found disassociation between genetic divergence and sexual isolation, suggesting that they do not form necessarily a cause-effect duet. However, Albinaria voithii, the only dextral Albinaria species, shows strong sexual isolation against the other sinistral species. We discuss whether change in coiling either has triggered instantaneous speciation, or is an example of character displacement.     

Ecological speciation

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.     

From Russia with lobe: genetic differentiation in trilobed uncus Ostrinia spp. follows food plant, not hairy legs

Trilobed uncus taxa of the genus Ostrinia (Lepidoptera, Crambidae) illustrate the complex relationship, at early stages of speciation, between reproductive isolation and differentiation in morphology, resource use and genetic variation. On the basis of behaviour and ecology, we recently hypothesized that individuals with small mid-tibiae belong to two distinct species depending on host plant--O. nubilalis and O. scapulalis sensu Frolov et al. (2007) feeding on maize and on a number of dicotyledons, respectively. Individuals with small, medium or massive mid-tibiae would all belong to O. scapulalis as long as they feed on these dicotyledons. This contrasts with previous taxonomy, which distinguished three species by male mid-tibia morphology, regardless of host plant. Here, we test our hypothesis by examining the genetic structure of Ostrinia populations from regions with mid-tibia polymorphism--Western Russia and Kazakhstan--and comparing it with that of French populations where only small mid-tibiae occur. Results support two predictions: (1) maize- and dicotyledon-collected populations are genetically differentiated from each other like in France, and (2) dicotyledon-collected populations show no genetic evidence of consisting of more than one species. Between-species differentiation was unrelated to geographic distance, despite significant isolation by distance within species. The distinction between two and only two species differing by host plant thus holds at continental scale. Interestingly, one microsatellite locus contributed ～10 times more than the others to differentiation between both taxa. This deserves further investigation, as it might reveal a linkage between this outlier and loci involved in host-plant adaptation and/or reproductive isolation.     

Modeling the two‐locus architecture of divergent pollinator adaptation: how variation in SAD paralogs affects fitness and evolutionary divergence in sexually deceptive orchids

Divergent selection by pollinators can bring about strong reproductive isolation via changes at few genes of large effect. This has recently been demonstrated in sexually deceptive orchids, where studies (1) quantified the strength of reproductive isolation in the field; (2) identified genes that appear to be causal for reproductive isolation; and (3) demonstrated selection by analysis of natural variation in gene sequence and expression. In a group of closely related Ophrys orchids, specific floral scent components, namely n‐alkenes, are the key floral traits that control specific pollinator attraction by chemical mimicry of insect sex pheromones. The genetic basis of species‐specific differences in alkene production mainly lies in two biosynthetic genes encoding stearoyl–acyl carrier protein desaturases (SAD) that are associated with floral scent variation and reproductive isolation between closely related species, and evolve under pollinator‐mediated selection. However, the implications of this genetic architecture of key floral traits on the evolutionary processes of pollinator adaptation and speciation in this plant group remain unclear. Here, we expand on these recent findings to model scenarios of adaptive evolutionary change at SAD2 and SAD5, their effects on plant fitness (i.e., offspring number), and the dynamics of speciation. Our model suggests that the two‐locus architecture of reproductive isolation allows for rapid sympatric speciation by pollinator shift; however, the likelihood of such pollinator‐mediated speciation is asymmetric between the two orchid species O. sphegodes and O. exaltata due to different fitness effects of their predominant SAD2 and SAD5 alleles. Our study not only provides insight into pollinator adaptation and speciation mechanisms of sexually deceptive orchids but also demonstrates the power of applying a modeling approach to the study of pollinator‐driven ecological speciation.     

Intraspecific Colour Variation among Lizards in Distinct Island Environments Enhances Local Camouflage

Within-species colour variation is widespread among animals. Understanding how this arises can elucidate evolutionary mechanisms, such as those underlying reproductive isolation and speciation. Here, we investigated whether five island populations of Aegean wall lizards (Podarcis erhardii) have more effective camouflage against their own (local) island substrates than against other (non-local) island substrates to avian predators, and whether this was linked to island differences in substrate appearance. We also investigated whether degree of local substrate matching varied among island populations and between sexes. In most populations, both sexes were better matched against local backgrounds than against non-local backgrounds, particularly in terms of luminance (perceived lightness), which usually occurred when local and non-local backgrounds were different in appearance. This was found even between island populations that historically had a land connection and in populations that have been isolated relatively recently, suggesting that isolation in these distinct island environments has been sufficient to cause enhanced local background matching, sometimes on a rapid evolutionary time-scale. However, heightened local matching was poorer in populations inhabiting more variable and unstable environments with a prolonged history of volcanic activity. Overall, these results show that lizard coloration is tuned to provide camouflage in local environments, either due to genetic adaptation or changes during development. Yet, the occurrence and extent of selection for local matching may depend on specific conditions associated with local ecology and biogeographic history. These results emphasize how anti-predator adaptations to different environments can drive divergence within a species, which may contribute to reproductive isolation among populations and lead to ecological speciation.     

植物物种形成的模式与机制

物种形成是指由已有的物种通过各种进化机制进化出新物种的过程。持续不断的物种形成产生了地球上灿烂的生物物种多样性。然而,研究人员对物种形成的模式与机制的了解却非常有限。一直以来,谱系分裂被认为是最重要的物种形成模式,但在植物中,谱系融合,即通过杂交形成新物种的过程,也是一个非常重要的物种形成模式。经过几十年的研究才逐渐认识到,生殖隔离是差异适应和遗传漂变的副产品,而不是物种形成的前提。相比合子形成后隔离,合子形成前的隔离在物种形成过程中更早地发挥作用。合子形成前的隔离,尤其是生态地理的隔离是植物中最重要的隔离机制。一些基于QTLs分析的研究发现,基因组中的少数主效位点在物种形成中起了关键作用,并且这些位点往往受到自然选择的作用。适应性辐射往往发生在隆起的山脉和新形成的岛屿上,很可能与这些地方能够提供很多可利用的生态位有关。最新的物种形成理论认为,基因是物种形成的基本单位,不同的物种可以在非控制物种差异适应性状的位点上存在基因流。这一观点为植物物种形成的研究提供了新的思路。随着植物物种形成研究的深入,越来越多植物物种形成基因被分离,包括花色素苷合成通路和S-基因座上的一些关键基因,揭示了植物物种形成的分子机制。前期的研究主要集中在模式植物和农作物上,许多生态上非常有趣的非模式植物还未得到广泛的研究。在未来的研究中,还需要更多来自非模式植物的例子以全面理解植物物种形成的多样化机制。