Pattern,process and geographic modes of speciation

The tradition of classifying cases of speciation into discrete geographic categories (allopatric, parapatric and sympatric) fuelled decades of fruitful research and debate. Not surprisingly, as the science has become more sophisticated, this simplistic taxonomy has become increasingly obsolete. Geographic patterns are now reasonably well understood. Sister species are rarely sympatric, implying that sympatric speciation, it its most general sense, is rare. However, sympatric speciation, even in its most restricted population genetic sense, is possible. Several case studies have demonstrated that divergence has occurred in nature without geographic barriers to gene flow. Obviously, different sets of criteria for sympatric speciation will lead to different numbers of qualifying cases. But changing the rules of nomenclature to make ‘sympatric speciation’ more or less common does not constitute scientific progress. Advances in the study of speciation have come from studies of the processes that constrain or promote divergence, and how they are affected by geography.     

Heteropatric speciation in a duck,Anas crecca

Heteropatric differentiation is a mode of speciation with gene flow in which divergence occurs between lineages that are in sympatry and allopatry at different times during cyclic spatial movements. Empirical evidence suggests that heteropatric differentiation may prove to be common among seasonally migratory organisms. We examined genetic differentiation between the sedentary Aleutian Islands population of green‐winged teal (Anas crecca‐nimia) and its close migratory relative, the Eurasian, or Old World (OW), Anas c. crecca population, a portion of which passes through the range of nimia during its seasonal migrations. We also examined its relationship with the parapatric North American, New World (NW), A. c. carolinensis population. Sequence data from eight nuclear introns and the mtDNA control region showed that the nimia‐crecca divergence occurred much more recently than the deeper crecca‐carolinensis split (~83 000 years vs. ~1.1 Myr). Despite considerable spatial overlap between crecca and nimia during seasonal migration, three key predictions of heteropatric differentiation are supported: significant genetic divergence (overall mean Φ_st  = 0.07), low gene flow (2N_em ~ 1.8), and an effective population size in nimia that is not especially low (N_e ~ 80 000 individuals). Similar levels of gene flow have come into nimia from carolinensis, but no detectable nuclear gene flow has gone out of nimia into either OW (crecca) or NW (carolinensis) populations. We infer that adaptations of these populations to local optima in different places (e.g. each matching their reproductive effort to different resource blooms) promote genetic isolation and divergence despite periods of sympatry between them, as the heteropatric model predicts.     

What,if anything,is sympatric speciation?

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

The genomics of adaptation,divergence and speciation: a congealing theory

In this issue, Flaxman et al. ( 2014 ) report the results of sophisticated whole‐genome simulations of speciation with gene flow, enhancing our understanding of the process by building on previous single‐locus, multilocus and analytical works. Their findings provide us with new insights about how genomes can diverge and the importance of statistical and chromosomal linkage in facilitating reproductive isolation. The authors characterize the conditions under which, even with high gene flow and weak divergent selection, reproductive isolation between populations can occur due to the emergent stochastic process of genomewide congealing, where numerous statistically or physically linked loci of small effect allow selection to limit effective migration rates. The initial congealing event can occur within a broad range conditions, and once initiated, the self‐reinforcing process leads to rapid divergence and ultimately two reproductively isolated populations. Flaxman et al.'s ( 2014 ) work is a valuable contribution to our understanding of speciation with gene flow and in making a more predictive field of evolutionary genomics and speciation.     

Cryptic speciation along a bathymetric gradient

The deep ocean supports a highly diverse and mostly endemic fauna, yet little is known about how or where new species form in this remote ecosystem. How speciation occurs is especially intriguing in the deep sea because few obvious barriers exist that would disrupt gene flow. Geographic and bathymetric patterns of genetic variation can provide key insights into how and where new species form. We quantified the population genetic structure of a protobranch bivalve, Neilonella salicensis, along a depth gradient (2200–3800 m) in the western North Atlantic using both nuclear (28S and calmodulin intron) and mitochondrial (cytochrome c oxidase subunit I) loci. A sharp genetic break occurred for each locus between populations above 2800 m and below 3200 m, defining two distinct clades with no nuclear or mitochondrial haplotypes shared between depth regimes. Bayesian phylogenetic analyses provided strong support for two clades, separated by depth, within N. salicensis. Although no morphological divergence was apparent, we suggest that the depth‐related population genetic and phylogenetic divergence is indicative of a cryptic species. The frequent occurrence of various stages of divergence associated with species formation along bathymetric gradients suggests that depth, and the environmental gradients that attend changes in depth, probably play a fundamental role in the diversification of marine organisms, especially in deep water. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 897–913.     

A parapatric propensity for breeding precludes the completion of speciation in common teal (Anas crecca, sensu lato)

Speciation is a process in which genetic drift and selection cause divergence over time. However, there is no rule dictating the time required for speciation, and even low levels of gene flow hinder divergence, so that taxa may be poised at the threshold of speciation for long periods of evolutionary time. We sequenced mitochondrial DNA (mtDNA) and eight nuclear introns (nuDNA) to estimate genomic levels of differentiation and gene flow between the Eurasian common teal (Anas crecca crecca) and the North American green‐winged teal (Anas crecca carolinensis). These ducks come into contact in Beringia (north‐eastern Asia and north‐western North America) and have probably done so, perhaps cyclically, since the Pliocene–Pleistocene transition, ～2.6 Ma, when they apparently began diverging. They have diagnosable differences in male plumage and are 6.9% divergent in the mtDNA control region, with only 1 of 58 crecca and 2 of 86 carolinensis having haplotypes grouping with the other. Two nuclear loci were likewise strongly structured between these teal (Φ_st ≥ 0.35), but six loci were undifferentiated or only weakly structured (Φ_st = 0.0–0.06). Gene flow between crecca and carolinensis was ～1 individual per generation in both directions in mtDNA, but was asymmetrical in nuDNA, with ～1 and ～20 individuals per generation immigrating into crecca and carolinensis, respectively. This study illustrates that species delimitation using a single marker oversimplifies the complexity of the speciation process, and it suggests that even with divergent selection, moderate levels of gene flow may stall the speciation process short of completion.     

The genetic basis of evolution, adaptation and speciation

A primary question in biology concerns the genetic basis of the evolution of novel traits, often in response to environmental changes, and how this can subsequently cause species isolation. This topic was the focus of the symposium on the Genetics of Speciation and Evolution at the annual meeting of the Canadian Society for Ecology and Evolution, held in Banff in May 2011. The presentations revealed some of the rapid advances being made in understanding the genetic basis of adaptation and speciation, as well as the elegant interplay between an organism's genetic complement and the environment that organism experiences.     

Mutualism, hybrid inviability and speciation in a tropical ant-plant

Although biotic interactions are particularly intricate in the tropics, few studies have examined whether divergent adaptations to biotic interactions lead to speciation in tropical organisms. Ant-plant mutualisms are widespread in the tropics. Within Leonardoxa africana, two subspecies present contrasting defences against herbivores. Young leaves of subsp. africana are defended by mutualistic ants, whereas subsp. gracilicaulis satiates herbivores by synchronized leaf production. Subsp. africana possesses hollow internodes and many large foliar nectaries, housing and feeding ants. We detected no genetic introgression between the two subspecies in the contact zone between them. F1 hybrids were present. They were intermediate in phenotype, expressing reduced, nonfunctional but costly myrmecophilic traits. However, they suffered more herbivory than their parents. Hybrids remained small, failing to reach reproductive size, probably due to their maladapted defence phenotype. Hence, there could be a direct link between adaptation to mutualism and reproductive isolation: biotic interactions could be a driver of tropical diversity.     

Conditions for mutation-order speciation

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.     

Genealogical footprints of speciation processes in wild tomatoes: demography and evidence for historical gene flow

Multilocus studies assessing patterns of nucleotide polymorphism within and among closely related species provide access to genealogical information bearing on demographic and geographic aspects of their speciation history. However, the technical difficulties in obtaining sufficient sequence data have severely limited this approach thus far, especially in outbred plant taxa. We employ the analytical framework of divergence population genetics in testing the isolation model of speciation in three self-incompatible species of wild tomatoes (clade Lycopersicon), in particular the assumption of divergence without gene flow. Based on DNA sequence data for 13 nuclear loci, average levels of silent polymorphism vary more than three-fold among species. We estimate a large effective population size for the ancestral species, quite similar to that of the highly polymorphic L. peruvianum. The other two species, however, exhibit concordant signatures of population-size reduction. These demographic inferences are biologically plausible and consistent with results obtained from standard neutrality tests. While the isolation model cannot be rejected by goodness-of-fit criteria, patterns of intragenic linkage disequilibrium in L. peruvianum are indicative of historical introgression at least in some regions of the genome. Considered jointly with the geographic pattern of postzygotic reproductive isolation, our results suggest that speciation occurred under residual gene flow, implying natural selection as one of the evolutionary forces driving the diversification of tomato lineages.     

Dispersal and the transition to sympatry in vertebrates

Under allopatric speciation models, a key step in the build-up of species richness is population dispersal leading to the co-occurrence of previously geographically isolated forms. Despite its central importance for community assembly, the extent to which the transition from spatial segregation (allopatry or parapatry) to coexistence (sympatry) is a predictable process, or alternatively one governed by chance and the vagaries of biogeographic history, remains poorly understood. Here, we use estimated divergence times and current patterns of geographical range overlap among sister species to explore the evolution of sympatry in vertebrates. We show that rates of transition to sympatry vary predictably according to ecology, being faster in marine or strongly dispersive terrestrial clades. This association with organism vagility is robust to the relative frequency of geographical speciation modes and consistent across taxonomic scales and metrics of dispersal ability. These findings reject neutral models of dispersal assembly based simply on evolutionary age and are not predicted by the main alternative view that range overlap is primarily constrained by biotic interactions. We conclude that species differences in dispersal limitation are fundamental in organizing the assembly of ecological communities and shaping broad-scale patterns of biodiversity over space and time.     

Climatic adaptation and ecological divergence between two closely related pine species in Southeast China

Climate is one of the most important drivers for adaptive evolution in forest trees. Climatic selection contributes greatly to local adaptation and intraspecific differentiation, but this kind of selection could also have promoted interspecific divergence through ecological speciation. To test this hypothesis, we examined intra‐ and interspecific genetic variation at 25 climate‐related candidate genes and 12 reference loci in two closely related pine species, Pinus massoniana Lamb. and Pinus hwangshanensis Hisa, using population genetic and landscape genetic approaches. These two species occur in Southeast China but have contrasting ecological preferences in terms of several environmental variables, notably altitude, although hybrids form where their distributions overlap. One or more robust tests detected signals of recent and/or ancient selection at two‐thirds (17) of the 25 candidate genes, at varying evolutionary timescales, but only three of the 12 reference loci. The signals of recent selection were species specific, but signals of ancient selection were mostly shared by the two species likely because of the shared evolutionary history. F_ST outlier analysis identified six SNPs in five climate‐related candidate genes under divergent selection between the two species. In addition, a total of 24 candidate SNPs representing nine candidate genes showed significant correlation with altitudinal divergence in the two species based on the covariance matrix of population history derived from reference SNPs. Genetic differentiation between these two species was higher at the candidate genes than at the reference loci. Moreover, analysis using the isolation‐with‐migration model indicated that gene flow between the species has been more restricted for climate‐related candidate genes than the reference loci, in both directions. Taken together, our results suggest that species‐specific and divergent climatic selection at the candidate genes might have counteracted interspecific gene flow and played a key role in the ecological divergence of these two closely related pine species.     

Ecological speciation in dynamic landscapes

Although verbal theories of speciation consider landscape changes, ecological speciation is usually modelled in a fixed geographical arrangement. Yet landscape changes occur, at different spatio-temporal scales, due to geological, climatic or ecological processes, and these changes result in repeated divisions and reconnections of populations. We examine the effect of such landscape dynamics on speciation. We use a stochastic, sexual population model with polygenic inheritance, embedded in a landscape dynamics model (allopatry-sympatry oscillations). We show that, under stabilizing selection, allopatry easily generates diversity, but species coexistence is evolutionarily unsustainable. Allopatry produces refuges whose persistence depends on the characteristic time scales of the landscape dynamics. Under disruptive selection, assuming that sympatric speciation is impossible due to Mendelian inheritance, allopatry is necessary for ecological differentiation. The completion of reproductive isolation, by reinforcement, then requires several sympatric phases. These results demonstrate that the succession of past, current and future geographical arrangements considerably influence the speciation process.     

Inferring the mode of speciation in Indo-West Pacific Conus (Gastropoda: Conidae)

Aim This study aims to initially explore the mode of speciation in Indo‐West Pacific Conus. Location The Indo‐West Pacific island arc, Indian and Pacific Oceans. Methods Relating evolutionary divergence in a molecular phylogeny [T.F. Duda & S.R. Palumbi (1999) Proceedings of the National Academy of Science USA, 96 , 10272] using node height with modern range extents as a possible measure of allopatric or sympatric speciation following that of T.G. Barraclough, A.P. Vogler & P.H. Harvey [(1999) Evolution of Biological Diversity. Oxford University Press, Oxford] models of sympatric and allopatric speciation. Results The analysis seems to indicate that the relationship of sympatry with node height is not informative. Species that have diverged quite recently show 100% sympatry with the sister species. A clearer signal of recent allopatric speciation is observed in species whose distribution is at the edge of the Indian and Pacific Ocean basins. In the widely distributed Conus ebraeus clade, the relationships of node heights and range extents of the member species support a key prediction of sympatric speciation. In highly ecologically specialized species, there is a smaller degree of sympatry than those species that are less specialized. Main conclusions The modes of speciation models presented in this study are not informative. This suggests that there had been large and possibly rapid changes in range size after speciation in the various clades. This could have been due to the fact that the wide dispersal life‐history strategy in the genus had been largely conserved in Conus evolution. There is evidence of sympatric and parapatric speciation in one Conus clade. Overall, the patterns of phylogeny and range distribution when related to the timing of speciation lend circumstantial support to a Neogene centre of origin hypothesis but not to speciation on the Pacific Plate. Speciation is likely to have been associated with the Tethys Sea closure event, with rapid speciation occurring after closure.     

Morphological divergence and the Quaternary speciation of Actaea purpurea (Ranunculaceae) and its relatives

To understand the process and mechanism of speciation, a detailed analysis of origin and demographic history of recently diverged species pairs is necessary. Here, we investigate the evolutionary history of Actaea purpurea (P.K. Hsiao) J. Compton and its closest relatives, A. japonica Thunb. and A. biternata (Siebold and Zuccarini) Prantl. We aim to estimate important parameters of the divergence event, and to lay the foundation for further investigation of the speciation mechanism of this system. Floral and vegetative traits were measured and analyzed. Genetic structure, divergence history, and historical gene flow were also inferred from the plastid and single nucleotide polymorphism data. Floral traits were divergent, and a strong match between pollinator and floral traits was revealed. Genetically the two species were also well diverged, and the time of divergence was dated to the Pleistocene. The demographic modelling results suggest that A. purpurea had continuous limited gene flow with A. japonica and A. biternata since divergence. More work is now needed to confirm that floral trait divergence was selected by pollinators, as well as to understand how pollinator isolation acts in conjunction with other reproductive barriers to reduce gene flow between the two species.     

Hitching a lift on the road to speciation

Understanding how speciation can take place in the presence of homogenizing gene flow remains a major challenge in evolutionary biology. In the early stages of ecological speciation, reproductive isolation between populations occupying different habitats is expected to be concentrated around genes for local adaptation. These genomic regions will show high divergence while gene exchange in other regions of the genome should continue relatively unimpaired, resulting in low levels of differentiation. The problem is to explain how speciation progresses from this point towards complete reproductive isolation, allowing genome‐wide divergence. A new study by Via and West (2008) on speciation between host races of the pea aphid, Acyrthosiphon pisum, introduces the mechanism of ‘divergence hitchhiking’ which can generate large ‘islands of differentiation’ and facilitate the build‐up of linkage disequilibrium, favouring increased reproductive isolation. This idea potentially removes a major stumbling block to speciation under continuous gene flow.     

物种形成过程中的分化基因组岛及其形成机制

理解物种形成机制是生态和进化领域的重要任务。得益于测序技术的快速发展, 越来越多研究发现分化种群(亚种、物种)间的基因组常呈现异质性分化景观, 存在分化基因组岛, 这被认为是基因流存在下的歧化选择引起的, 支持基因流存在下的成种假说。然而, 基因渐渗、祖先多态性的差异分选、连锁选择等其他进化过程也可导致分化基因组岛的形成。现有实证研究在解析分化基因组岛的形成机制时, 往往忽略了上述其他进化过程的作用。为此, 本文在辨析分化基因组岛相关概念的基础上, 总结了利用种群基因组数据鉴定分化基因组岛的方法, 对比了不同进化过程形成分化基因组岛的特征, 指出在区分不同机制时联用基因渐渗程度、绝对分化指数(d_XY)、相对节点深度(RND)、重组率等多个指标的必要性, 归纳了物种形成过程中分化基因组岛形成机制解析的研究思路, 并对未来在生殖隔离机制上的深入探索以及实证研究的整合分析等方面进行了展望。     

Making inferences about speciation using sophisticated statistical genetics methods: look before you leap

Understanding speciation is a fundamental aim of evolutionary biology and a very challenging one. Speciation can be viewed as the dynamics of genetic differentiation between populations resulting in substantial reproductive isolation (Gavrilets 2003). It was generally accepted that very small levels of migration prevent genetic differentiation among populations and, therefore, speciation. However, recent theoretical work showed that sympatric speciation is possible (Gavrilets 2003). Nevertheless, providing empirical evidence that gene flow occurred during speciation is challenging because several gene flow scenarios can explain observed patterns of genetic differentiation. Positive migration rate estimates alone do not prove ongoing gene flow during divergence. We also need to know whether migration took place before, during or after speciation. There is no statistical method specifically aimed at estimating gene flow timing, but several studies used the isolation with migration model (Hey & Nielsen 2004, 2007; Hey 2010b) to estimate this parameter and make inferences about speciation scenarios. It is tempting to use statistical methods to estimate important evolutionary parameters even if they do not appear explicitly in the inference model. Nevertheless, before doing so, we need to determine whether they can provide reliable results. In this issue of Molecular Ecology, Strasburg and Rieseberg (2011) present a simulation study that examines the degree to which gene flow timing estimates obtained from IMa2 (Hey 2010b) can be used to make inferences about speciation mode. Their results are sobering; gene flow timing estimates obtained in this way are not reliable and cannot be used to unequivocally establish if gene flow was ongoing during speciation.