Incipient Speciation

The study of speciation is concerned with understanding the connection between causes of divergent evolution and the origin and maintenance of barriers to gene exchange between incipient species. Although the field has historically focused either on examples of recent divergence and its causes or on the genetic basis of reproductive isolation between already divergent species, current efforts seek to unify these two approaches. Here we integrate these perspectives through a discussion of recent progress in several insect speciation model systems. We focus on the evolution of speciation phenotypes in each system (i.e., those phenotypes causally involved in reducing gene flow between incipient species), drawing an explicit connection between cause and effect (process and pattern). We emphasize emerging insights into the genomic architecture of speciation as well as timely areas for future research.

Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near‐instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate spec...

Despite persistent debate on the nature of species, the widespread adoption of Mayr's biological species concept has led to a heavy emphasis on the importance of reproductive isolation to the speciation process. Equating the origin of species with the evolution of reproductive isolation has become common practice in the study of speciation, coincident with an increasing focus on elucidating the specific genetic changes (i.e.-speciation genes) underlying intrinsic reproductive barriers between species. In contrast, some have recognized that reproductive isolation is usually a signature effect rather than a primary cause of speciation. Here we describe a research paradigm that shifts emphasis from effects to causes in order to resolve this apparent contradiction and galvanize the study of speciation. We identify major elements necessary for a balanced and comprehensive investigation of the origin of species and place the study of so-called ''speciation genes'' into its appropriate context. We emphasize the importance of characterizing diverging phenotypes, identifying relevant evolutionary forces acting on those phenotypes and their role in the causal origins of reduced gene flow between incipient species, and the nature of the genetic and phenotypic boundaries that results from such processes. This approach has the potential to unify the field of speciation research, by allowing us to make better ''historical'' predictions about the fate of diverging populations regardless of taxon.

Perumytilus purpuratus is a mussel species that is broadly distributed along the latitudinal gradient from the Southern Pacific to the Atlantic Ocean. Along its distribution, P. purpuratus has been historically considered as one species. However, in the last decade, evidence has supported the hypothesis of two geographically divergent lineages. Within this context, we explore the evolutionary history of this inter-oceanic mussel, linking both sperm acrosome variability and molecular analyses of males at the geographic macroscale. In general, our results were in agreement with the genetic divergence that was previously reported, and showing two north and south lineage. Furthermore, our comprehensive sampling effort enabled us to precisely determine both the latitudinal positions of morpho-genetic break, which was identified at 37 • S on the Pacific coast, and a probable hybridization zone at 38 • S. In addition, we found new southern sperm variants, longer than previously reported. Overall, our results support the hypothesis of historical events and postglacial recolonization as causal phenomena for the observed divergences. Finally, we consider that, despite uncertainties in the taxonomy of P. purpuratus, the morpho-genetic divergence between the north and south P. purpuratus lineages indicates that they do not constitute the same Evolutionary Significant Unit and, therefore, they should be considered as separate entities.

Data accessibility: Java source codes for the individual-based evolutionary simulations, R scripts to analyze and visualize simulation results, and final output files of all simulations presented in this article are available in the Dryad repository doi:10.5061/dryad.7sqv9s4pw).

Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known. We previously explored the genomics of very recent ecological speciation into lake and stream ecotypes in stickleback from Lake Constance. Here, we reconstruct the origin of alleles underlying ecological speciation by combining demographic modelling on genome-wide single nucleotide polymorphisms, phenotypic data and mitochondrial sequence data in the wider European biogeographical context. We find that parallel differentiation between lake and stream ecotypes across replicate lake-stream ecotones resulted from recent secondary contact and admixture between old East and West European lineages. Unexpectedly, West European alleles that introgressed across the hybrid zone at the western end of the lake, were recruited to genomic islands of differentiation between ecotypes at the eastern end of the lake. Our results highlight an overlooked outcome of secondary contact: ecological speciation facilitated by admixture variation.

We investigate extensive quantitative trait variation (dewlap hue, colour pattern, dorsum hue, body proportions and scalation) in the Martinique anole across eight transects representing nascent parapatric ecological speciation, nascent allopatric speciation and allopatric divergence without sufficient genetic structure to suggest speciation. Quantitative trait divergence can be extremely large between adjacent sets of populations, but with one exception that this is associated with difference in habitat rather than past allopatry. Nascent ecological speciation shows the greatest level of quantitative trait divergence across all character sets including those implicated in natural, as well as sexual selection. The sole example of nascent allopatric speciation is associated with fairly strong quantitative trait divergence among most character sets, but not the set most implicated in natural (rather than sexual) selection. The role of sexual selection in ecological speciation is discu...

The biogeographic patterns in sexually reproducing animals in island archipelagos may be interpreted as reflecting the importance of allopatric speciation. However, as the forms are allopatric, their reproductive isolation is largely untestable. A historical perspective integrating geology and molecular phylogeny reveals specific cases where ancient precursor islands coalesce, which allows the application of population genetics to critically test genetic isolation. TheAnolispopulations on Martinique in the Lesser Antilles are one such case where species-level populations on ancient precursor islands (ca6–8 Myr BP) have met relatively recently. The distribution of the mtDNA lineages is tightly linked to the precursor island, but the population genetic analysis of microsatellite variation in large samples shows no evidence of restricted genetic exchange between these forms in secondary contact. This tests, and rejects, the hypothesis of simple allopatric speciation in these forms. By ...

Morphological divergence was evident among three sympatric morphs of Arctic charr (Salvelinus alpinus (L.)) that are ecologically diverged along the shallow-, deep-water resource axis in a subarctic postglacial lake (Norway). The two deep-water (profundal) spawning morphs, a benthivore (PB-morph) and a piscivore (PP-morph), have evolved under identical abiotic conditions with constant low light and temperature levels in their deep-water habitat, and were morphologically most similar. However, they differed in important head traits (e.g., eye and mouth size) related to their different diet specializations. The small-sized PB-morph had a paedomorphic appearance with a blunt head shape, large eyes, and a deep body shape adapted to their profundal lifestyle feeding on submerged benthos from soft, deep-water sediments. The PP-morph had a robust head, large mouth with numerous teeth, and an elongated body shape strongly related to their piscivorous behavior. The littoral spawning omnivore morph (LO-morph) predominantly utilizes the shallow benthicpelagic habitat and food resources. Compared to the deep-water morphs, the LO-morph had smaller head relative to body size. The LO-morph exhibited traits typical for both shallow-water benthic feeding (e.g., large body depths and small eyes) and planktivorous feeding in the pelagic habitat (e.g., streamlined body shape and small mouth). The development of morphological differences within the same deep-water habitat for the PB-and PP-morphs highlights the potential of biotic factors and ecological interactions to promote further divergence in the evolution of polymorphism in a tentative incipient speciation process. The diversity of deep-water charr in this study represents a novelty in the Arctic charr polymorphism as a truly deep-water piscivore morph has to our knowledge not been described elsewhere.

Sensory cues exchanged during courtship are crucial for mate choice: if they show intraspecific divergence, this may cause or reinforce sexual isolation between strains, ultimately leading to speciation. There is a strong asymmetric sexual isolation between Drosophila melanogaster females from Zimbabwe (Z) and males from all other populations (M). While M and Z flies of both sexes show different cuticular pheromones, this variation is only partly responsible for the intraspecific isolation effect. Male acoustic signals are also partly involved in sexual isolation. We examined strain-specific courtship behaviour sequences to determine which body parts and sensory appendages may be involved in sexual isolation. Using two strains representative of the Z-and M-types, we manipulated sensory cues and the social context; we then measured the consequence of these manipulations on courtship and copulation. Our data suggest that Z females mated best with males whose sensory characteristics matched those of Z males in both quantity and quality. M females were less choosy and much less influenced by the sensory and social contexts. Differences in emission and reception of sensory signals seen between Z and M flies may lead to the concerted evolution of multiple sensory channel, thereby shaping a population-specific mate recognition system.

Box-and-whisker plots indicate the courtship index (during a 10 min period) measured in homo- and heterotypic pairs combining Z6 and/or AL flies, under white (W) or red light (R) conditions (see at the bottom of the graphs). Courtship index were measured with intact (A) or beheaded females (B) and courtship latency with intact females (C). These parameters were compared using the Kruskal-Wallis test. The letters above the whisker indicate statistical differences. For each pair and condition, N = 46 – 57.

Explaining how and why reproductive isolation evolves and determining which forms of reproductive isolation have the largest impact on the process of population divergence are major goals in the study of speciation. By studying recent adaptive radiations in incompletely isolated taxa, it is possible to identify barriers involved at early divergence before other confounding barriers emerge after speciation is complete. Sibling species of the complex offer opportunities to provide insights into speciation mechanisms. Here, we studied patterns of reproductive isolation among three taxa, , . and , to compare its strength at different spatial scales, to dissect the relative contribution of pre- versus postmating isolation, and to infer the involvement of ecological divergence on hybridization. Because F1 hybrids are viable, fertile and not uncommon, understanding the dynamics of hybridization in this trio of major malaria vectors has important implications for how adaptations arise and s...

The main Afrotropical malaria vector, Anopheles gambiae sensu stricto, is undergoing a process of sympatric ecological diversification leading to at least two incipient species (the M and S molecular forms) showing heterogeneous levels of divergence across the genome. The physically unlinked centromeric regions on all three chromosomes of these closely related taxa contain fixed nucleotide differences which have been found in nearly complete linkage disequilibrium in geographic areas of no or low M-S hybridization. Assays diagnostic for SNP and structural differences between M and S forms in the three centromeric regions were applied in samples from the western extreme of their range of sympatry, the only area where high frequencies of putative M/S hybrids have been reported. The results reveal a level of admixture not observed in the rest of the range. In particular, we found: i) heterozygous genotypes at each marker, although at frequencies lower than expected under panmixia; ii) virtually all possible genotypic combinations between markers on different chromosomes, although genetic association was nevertheless detected; iii) discordant M and S genotypes at two X-linked markers near the centromere, suggestive of introgression and inter-locus recombination. These results could be indicative either of a secondary contact zone between M and S, or of the maintenance of ancestral polymorphisms. This issue and the perspectives opened by these results in the study of the M and S incipient speciation process are discussed.

Perumytilus purpuratus is a mussel species that is broadly distributed along the latitudinal gradient from the Southern Pacific to the Atlantic Ocean. Along its distribution, P. purpuratus has been historically considered as one species. However, in the last decade, evidence has supported the hypothesis of two geographically divergent lineages. Within this context, we explore the evolutionary history of this inter-oceanic mussel, linking both sperm acrosome variability and molecular analyses of males at the geographic macroscale. In general, our results were in agreement with the genetic divergence that was previously reported, and showing two north and south lineage. Furthermore, our comprehensive sampling effort enabled us to precisely determine both the latitudinal positions of morpho-genetic break, which was identified at 37 • S on the Pacific coast, and a probable hybridization zone at 38 • S. In addition, we found new southern sperm variants, longer than previously reported. Overall, our results support the hypothesis of historical events and postglacial recolonization as causal phenomena for the observed divergences. Finally, we consider that, despite uncertainties in the taxonomy of P. purpuratus, the morpho-genetic divergence between the north and south P. purpuratus lineages indicates that they do not constitute the same Evolutionary Significant Unit and, therefore, they should be considered as separate entities.

Perumytilus purpuratus is a mussel species that is broadly distributed along the latitudinal gradient from the Southern Pacific to the Atlantic Ocean. Along its distribution, P. purpuratus has been historically considered as one species. However, in the last decade, evidence has supported the hypothesis of two geographically divergent lineages. Within this context, we explore the evolutionary history of this inter-oceanic mussel, linking both sperm acrosome variability and molecular analyses of males at the geographic macroscale. In general, our results were in agreement with the genetic divergence that was previously reported, and showing two north and south lineage. Furthermore, our comprehensive sampling effort enabled us to precisely determine both the latitudinal positions of morpho-genetic break, which was identified at 37 • S on the Pacific coast, and a probable hybridization zone at 38 • S. In addition, we found new southern sperm variants, longer than previously reported. Overall, our results support the hypothesis of historical events and postglacial recolonization as causal phenomena for the observed divergences. Finally, we consider that, despite uncertainties in the taxonomy of P. purpuratus, the morpho-genetic divergence between the north and south P. purpuratus lineages indicates that they do not constitute the same Evolutionary Significant Unit and, therefore, they should be considered as separate entities.

The sibling species An. coluzzii and An. gambiae s.s. are major malaria vectors thought to be undergoing sympatric speciation with gene flow. In the absence of intrinsic post-zygotic isolation between the two taxa, speciation is thought possible through the association of assortative mating and genomic regions protected from gene flow by recombination suppression. Such genomic islands of speciation have been described in pericentromeric regions of the X, 2L and 3L chromosomes. Spatial swarm segregation plays a major role in assortative mating between sympatric populations of the two species and, given their importance for speciation, genes responsible for such pre-mating reproductive barriers are expected to be protected within divergence islands. In this study 2063 male and 266 female An. coluzzii and An. gambiae s.s. individuals from natural swarms in Burkina Faso, West Africa were sampled. These were genotyped at 16 speciation island SNPs, and characterized as non-hybrid individu...

Background In the speciation continuum, the strength of reproductive isolation varies, and species boundaries are blurred by gene flow. Interbreeding among giraffe (Giraffa spp.) in captivity is known, and anecdotal reports of natural hybrids exist. In Kenya, Nubian (G. camelopardalis camelopardalis), reticulated (G. reticulata), and Masai giraffe sensu stricto (G. tippelskirchi tippelskirchi) are parapatric, and thus, the country might be a melting pot for these taxa. We analyzed 128 genomes of wild giraffe, 113 newly sequenced, representing these three taxa. Results We found varying levels of Nubian ancestry in 13 reticulated giraffe sampled across the Laikipia Plateau most likely reflecting historical gene flow between these two lineages. Although comparatively weaker signs of ancestral gene flow and potential mitochondrial introgression from reticulated into Masai giraffe were also detected, estimated admixture levels between these two lineages are minimal. Importantly, contemporary gene flow between East African giraffe lineages was not statistically significant. Effective population sizes have declined since the Late Pleistocene, more severely for Nubian and reticulated giraffe. Conclusions Despite historically hybridizing, these three giraffe lineages have maintained their overall genomic integrity suggesting effective reproductive isolation, consistent with the previous classification of giraffe into four species.

Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near‐instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate spec...

Isolating barriers that drive speciation are commonly studied in the context of two-species hybrid zones. There is however evidence that more complex introgressive relationships are common in nature. Here, we use field observations and genomic analysis, including the sequencing and assembly of a novel reference genome, to study an emergent hybrid zone involving two colliding hybrid zones of three woodpecker species: Red-breasted, Red-naped, and Yellow-bellied Sapsuckers (Sphyrapicus ruber, S. nuchalis, and S. varius). Surveys of the area surrounding Prince George, British Columbia, Canada, show that all three species are sympatric, and Genotyping-by-Sequencing identifies hybrids from each species pair and birds with ancestry from all three species. Observations of mate pair phenotypes and genotypes provide evidence for assortative mating, though there is some heterospecific pairing. Hybridization is more extensive in this tri-species hybrid zone than in two di-species hybrid zones. ...

In a number of animal species, divergent natural selection has repeatedly and independently driven the evolution of reproductive isolation between populations adapted to contrasting, but not to similar environments1. This process is known as parallel ecological speciation, and examples in plants are enigmatically rare2. Here, we perform a comprehensive test of the ecological speciation hypothesis in an Australian wildflower where parapatric populations found in coastal sand dunes (Dune ecotype) and headlands (Headland ecotype) have repeatedly and independently diverged in growth habit. Consistent with a role for divergent natural selection driving the evolution of reproductive isolation, we found that Dune populations with erect growth habit were easy to transplant across sand dunes, were largely interfertile despite half-a-million years of divergence, and were reproductively isolated from equally divergent Headland populations with prostrate growth habit. However, we unexpectedly d...

Hybridization allows adaptations to be shared among lineages and may trigger the evolution of new species 1,2 . However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridization was crucial in generating reproductive isolation 3 . Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to examine a case of hybrid speciation in Heliconius butterflies. We show that Heliconius elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, Heliconius pardalinus, which homogenizes 99% of their genomes. The remaining 1% introgressed from the other parent, Heliconius melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands contain multiple traits that are under disruptive selection, including colour pattern, wing shape, host plant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits, and that speciation with gene flow is possible with a multilocus genetic architecture. Biodiversity has long been depicted as a 'tree of life', but a wealth of genomic data has made clear that the branches and leaves of the tree often do not represent neatly defined units. Instead, they comprise a braided delta of evolutionary lineages linked by hybridization and introgression 4 . Although gene flow tends to homogenize populations 5 , it may also contribute to adaptation and even drive speciation if introgressed variants cause reproductive isolation 1,2,6 . Polyploid (chromosome-doubling) hybrid speciation is common in plants , but compelling examples of homoploid hybrid speciation (without a change in chromosome number) remain scarce and contested, especially in animals 3 . This is because it is difficult to prove that hybridization had a pivotal role in creating reproductive isolation between the hybrid lineage and the parental species 3 . Here we present evidence for homoploid hybrid speciation in Heliconius butterflies. We show that introgression of key adaptive traits from H. melpomene caused H. elevatus to diverge from H. pardalinus, despite ongoing gene flow among sympatric H. elevatus and H. pardalinus, which homogenizes 99% of their genomes (Fig. ). Heliconius butterflies are chemically defended by cyanogenic glycosides, either sequestered from larval passion-vine host plants (Passifloraceae) or synthesized de novo . Adults signal their toxicity to predators through their brightly coloured wing patterns. The cost of educating predators is shared with other defended butterflies and moths through mutualistic Müllerian mimicry 11 . Mimicry among species is not restricted to colour pattern, because co-mimics also converge in flight behaviour and wing shape . Hybrids with intermediate phenotypes are selected against because predators do not recognize them . Therefore, different mimetic phenotypes correspond to fitness peaks in an adaptive landscape maintained by

Background In the speciation continuum, the strength of reproductive isolation varies, and species boundaries are blurred by gene flow. Interbreeding among giraffe (Giraffa spp.) in captivity is known, and anecdotal reports of natural hybrids exist. In Kenya, Nubian (G. camelopardalis camelopardalis), reticulated (G. reticulata), and Masai giraffe sensu stricto (G. tippelskirchi tippelskirchi) are parapatric, and thus, the country might be a melting pot for these taxa. We analyzed 128 genomes of wild giraffe, 113 newly sequenced, representing these three taxa. We found varying levels of Nubian ancestry in 13 reticulated giraffe sampled across the Laikipia Plateau most likely reflecting historical gene flow between these two lineages. Although comparatively weaker signs of ancestral gene flow and potential mitochondrial introgression from reticulated into Masai giraffe were also detected, estimated admixture levels between these two lineages are minimal. Importantly, contemporary gene flow between East African giraffe lineages was not statistically significant. Effective population sizes have declined since the Late Pleistocene, more severely for Nubian and reticulated giraffe. Conclusions Despite historically hybridizing, these three giraffe lineages have maintained their overall genomic integrity suggesting effective reproductive isolation, consistent with the previous classification of giraffe into four species.

Tibetan frogs, , are differentiated genetically but not morphologically along geographical and elevational gradients in a challenging environment, presenting a unique opportunity to investigate processes leading to speciation. Analyses of whole genomes of 63 frogs reveal population structuring and historical demography, characterized by highly restricted gene flow in a narrow geographic zone lying between matrilines West (W) and East (E). A population found only along a single tributary of the Yalu Zangbu River has the mitogenome only of E, whereas nuclear genes of W comprise 89-95% of the nuclear genome. Selection accounts for 579 broadly scattered, highly divergent regions (HDRs) of the genome, which involve 365 genes. These genes fall into 51 gene ontology (GO) functional classes, 14 of which are likely to be important in driving reproductive isolation. GO enrichment analyses of E reveal many overrepresented functional categories associated with adaptation to high elevations, inc...

Quantifying gene flow between lineages at different stages of the speciation continuum is central to understanding speciation.Heliconiusbutterflies have undergone an adaptive radiation in wing colour patterns driven partly by natural selection for local mimicry. Colour patterns are also known to be used as assortative mating cues. Therefore, wing pattern divergence is considered to play a role in speciation. A corollary is that mimicry between closely-related species may be associated with hybridization and interfere with reproductive isolation. Here, we take a multifaceted approach to explore speciation history, species boundaries, and traits involved in species differentiation between the two closely-related speciesH. hecaleandH. ismenius.We focus on geographic regions where the two species mimic each other, and contrast this with geographic regions where they do not mimic each other. To examine population history and patterns of gene flow, we tested and compared a four-population...

Significance Reproductive isolation is instrumental to the formation of new species (speciation), but it remains largely enigmatic how many incompatibilities are required to prevent hybridization and where they lie across the genome. By studying patterns of admixture in amphibian hybrid zones, we found that reproductive isolation is initiated by numerous small-effect incompatibilities scattered across the genome rather than concentrated in a few important genes. Unlike mammals and birds, in which Y/W degeneracy is a major cause of hybrid dysfunctions, the undifferentiated sex chromosomes of amphibians do not always host more genetic incompatibilities than other chromosomes. These combined results might explain why amphibian speciation is relatively slow, and its clock-like dynamics offer practical perspectives to categorize evolutionary lineages into species or subspecies.

Identifying mechanisms of speciation has proven one of the most challenging problems in evolutionary biology, perhaps mainly for two reasons, speciation is not readily accessible to experimental approaches, and rarely to time series analyses. Any one case of speciation can usually be investigated only at a single stage of completion. Cases of parallel ecological speciation driven repeatedly within the same taxon by divergent selection along replicate environmental gradients, have therefore received considerable attention (Schluter & Nagel 1995; Rundle et al. 2000). Several such systems have become major model systems in evolutionary ecology research, including sticklebacks in postglacial lakes (Rundle et al. 2000), Heliconius butterflies (Mallet et al. 1998), leaf beetles (Funk 1998) and Timema walking sticks (Nosil et al. 2002). They provide powerful means of identifying causes of divergence and may lend themselves to examining associations between variation in the environments and variation in the progress towards speciation (Nosil & Harmon, this volume). However, variation in the progress towards speciation among disconnected populations undergoing parallel speciation may be due to different contingency as much as different environments (Taylor & McPhail 2000). Ideally, to trace the correlates of the transition from panmixis to incipient speciation, one would want to study variation in the progress towards speciation in exactly the same pair of species, and along a continuous progress series, to minimize the potential confounding effect of variable historical contingency. The cichlid fish species Pundamilia pundamilia, Pundamilia nyererei, their hybrids and intermediate colour morphs occur at various stages of differentiation at different islands placed along an environmental gradient of water clarity in Lake Victoria. I will subsequently refer to this as a 'speciation transect'. At the same time, populations occurring at different islands do exchange genes as evident from microsatellite-allele frequencies (Seehausen et al. 2008), and also from several observed cases of invasion of, and establishment in, previously unoccupied islands within the 15 years time window that I have collected community Speciation and Patterns of Diversity, ed.

The role of natural selection in speciation, first described by Darwin, has finally been widely accepted. Yet, the nature and time course of the genetic changes that result in speciation remain mysterious. To date, genetic analyses of speciation have focused almost exclusively on retrospective analyses of reproductive isolation between species or subspecies and on hybrid sterility or inviability rather than on ecologically based barriers to gene flow. However, if we are to fully understand the origin of species, we must analyze the process from additional vantage points. By studying the genetic causes of partial reproductive isolation between specialized ecological races, early barriers to gene flow can be identified before they become confounded with other species differences. This population-level approach can reveal patterns that become invisible over time, such as the mosaic nature of the genome early in speciation. Under divergent selection in sympatry, the genomes of incipient...

In this contribution, the aspects of reptile and amphibian speciation that emerged from research performed over the past decade are reviewed. First, this study assesses how patterns and processes of speciation depend on knowing the taxonomy of the group in question, and discuss how integrative taxonomy has contributed to speciation research in these groups. This study then reviews the research on different aspects of speciation in reptiles and amphibians, including biogeography and climatic niches, ecological speciation, the relationship between speciation rates and phenotypic traits, and genetics and genomics. Further, several case studies of speciation in reptiles and amphibians that exemplify many of these themes are discussed. These include studies of integrative taxonomy and biogeography in South American lizards, ecological speciation in European salamanders, speciation and phenotypic evolution in frogs and lizards. The final case study combines genomics and biogeography in to...

It is now recognized that speciation can proceed even when divergent natural selection is opposed by gene flow. Understanding the extent to which environmental gradients and geographical distance can limit gene flow within species can shed light on the relative roles of selection and dispersal limitation during the early stages of population divergence and speciation. On the remote Lord Howe Island (Australia), ecological speciation with gene flow is thought to have taken place in several plant genera. The aim of this study was to establish the contributions of isolation by environment (IBE) and isolation by community (IBC) to the genetic structure of 19 plant species, from a number of distantly related families, which have been subjected to similar environmental pressures over comparable time scales. We applied an individual-based, multivariate, model averaging approach to quantify IBE and IBC, while controlling for isolation by distance (IBD). Our analyses demonstrated that all sp...

Interspecific studies indicate that sperm morphology and other ejaculatory traits diverge more rapidly than other types of character in Drosophila and other taxa. This pattern has largely been attributed to postcopulatory sexual selection involving interaction between the sexes. Such divergence has been suggested to lead rapidly to reproductive isolation among populations and thus to be an 'engine of speciation.' Here, we test two critical predictions of this hypothesis: (i) there is significant variation in reproductive traits among incipient species; and (ii) divergence in interacting sex-specific traits exhibits a coevolutionary pattern among populations within a species, by examining geographical variation in Drosophila mojavensis, a species in the early stages of speciation. Significant among-population variation was identified in sperm length and female sperm-storage organ length, and a strong pattern of correlated evolution between these interacting traits was observed. In addition, crosses among populations revealed coevolution of male and female contributions to egg size. Support for these two important predictions confirms that coevolving internal characters that mediate successful reproduction may play an important part in speciation. The next step is to determine exactly what that role is.

Understanding the drivers of speciation is fundamental in evolutionary biology, and recent studies highlight hybridization as a potential facilitator of adaptive radiations. Using whole-genome sequencing data from 22 species of guenons (tribe Cercopithecini), one of the world’s largest primate radiations, we show that rampant gene flow characterizes their evolutionary history, and identify ancient hybridization across deeply divergent lineages differing in ecology, morphology and karyotypes. Lineages experiencing gene flow tend to be more species-rich than non-admixed lineages. Mitochondrial transfers between distant lineages were likely facilitated by co-introgression of co-adapted nuclear variants. Although the genomic landscapes of introgression were largely lineage specific, we found that genes with immune functions were overrepresented in introgressing regions, in line with adaptive introgression, whereas genes involved in pigmentation and morphology may contribute to reproduct...

Small, isolated populations are prone to inbreeding, increasing the proportion of homozygous sites across the genome that can be quantified as runs of homozygosity (ROH). Caribou (Rangifer tarandus) are declining across their range in Canada; thus, understanding the effects of inbreeding on genetic potential is pertinent for conserving small, isolated populations. We quantified ROH in high-coverage whole genomes of boreal caribou from small, isolated populations in southern Ontario, Canada, in comparison to caribou from the continuous range of Ontario, other caribou ecotypes in Canada, and western Greenland. Sampled populations presented divergent evolutionary histories, differing population sizes, and extents of isolation. We conducted BLAST searches across regions of elevated heterozygosity to identify genes that have maintained variation despite inbreeding. We found caribou from recently isolated populations in Ontario had a large proportion of their genome in long ROH. We observ...

SUMMARYThe majority of the world population carry the gastric pathogenHelicobacter pylori. Fortunately, most individuals experience only low-grade or no symptoms, but in many cases the chronic inflammatory infection develops into severe gastric disease, including duodenal ulcer disease and gastric cancer. Here we report on a protective mechanism whereH. pyloriattachment and accompanying chronic mucosal inflammation can be reduced by antibodies that are present in a vast majority ofH. pyloricarriers. These antibodies block binding of theH. pyloriattachment protein BabA by mimicking BabA’s binding to the ABO blood group glycans in the gastric mucosa. However, many individuals demonstrate low titers of BabA blocking antibodies, which is associated with an increased risk for duodenal ulceration, suggesting a role for these antibodies in preventing gastric disease.

Background: Pallenopsis patagonica (Hoek, 1881) is a morphologically and genetically variable sea spider species whose taxonomic classification is challenging. Currently, it is considered as a species complex including several genetic lineages, many of which have not been formally described as species. Members of this species complex occur on the Patagonian and Antarctic continental shelves as well as around sub-Antarctic islands. These habitats have been strongly influenced by historical large-scale glaciations and previous studies suggested that communities were limited to very few refugia during glacial maxima. Therefore, allopatric speciation in these independent refugia is regarded as a common mechanism leading to high biodiversity of marine benthic taxa in the high-latitude Southern Hemisphere. However, other mechanisms such as ecological speciation have rarely been considered or tested. Therefore, we conducted an integrative morphological and genetic study on the P. patagonica species complex to i) resolve species diversity using a target hybrid enrichment approach to obtain multiple genomic markers, ii) find morphological characters and analyze morphometric measurements to distinguish species, and iii) investigate the speciation processes that led to multiple lineages within the species complex. Results: Phylogenomic results support most of the previously reported lineages within the P. patagonica species complex and morphological data show that several lineages are distinct species with diagnostic characters. Two lineages are proposed as new species, P. aulaeturcarum sp. nov. Dömel & Melzer, 2019 and P. obstaculumsuperavit sp. nov. Dömel, 2019, respectively. However, not all lineages could be distinguished morphologically and thus likely represent cryptic species that can only be identified with genetic tools. Further, morphometric data of 135 measurements showed a high amount of variability within and between species without clear support of adaptive divergence in sympatry.

Understanding the drivers of speciation is fundamental in evolutionary biology, and recent studies highlight hybridization as a potential facilitator of adaptive radiations. Using whole-genome sequencing data from 22 species of guenons (tribe Cercopithecini), one of the world’s largest primate radiations, we show that rampant gene flow characterizes their evolutionary history, and identify ancient hybridization across deeply divergent lineages differing in ecology, morphology and karyotypes. Lineages experiencing gene flow tend to be more species-rich than non-admixed lineages. Mitochondrial transfers between distant lineages were likely facilitated by co-introgression of co-adapted nuclear variants. Although the genomic landscapes of introgression were largely lineage specific, we found that genes with immune functions were overrepresented in introgressing regions, in line with adaptive introgression, whereas genes involved in pigmentation and morphology may contribute to reproduct...

Studies on parasite biogeography and host spectrum provide insights into the processes driving parasite diversification. Global geographical distribution and a multi-host spectrum make the tapewormLigula intestinalisa promising model for studying both the vicariant and ecological modes of speciation in parasites. To understand the relative importance of host association and biogeography in the evolutionary history of this tapeworm, we analysed mtDNA and reduced-represented genomic SNP data for a total of 139 specimens collected from 18 fish-host genera across a distribution range representing 21 countries. Our results strongly supported the existence of at least 10 evolutionary lineages and estimated the deepest divergence at approximately 4.99-5.05 Mya, which is much younger than the diversification of the fish host genera and orders. Historical biogeography analyses revealed that the ancestor of the parasite diversified following multiple vicariance events and was widespread throu...

Combining phylogeographic approaches and hybrid zone inference in a single framework is a robust way to depict respectively the biogeographic history of lineages and the evolutionary processes responsible for speciation. Here, we studied the spatiotemporal patterns of diversification and characterize the hybrid zone between two Atlantic Forest spinetails (Synallaxis ruficapilla and Synallaxis cinerea) using mitochondrial DNA and nuclear (autosomal and Z-linked) genes. We consistently recovered divergence between and within the two species during the late Pliocene and Pleistocene using an isolation with migration model. Also, our results indicate distinct levels of introgression among lineages. Ecological niche models and demographic inferences, used to infer range distributions throughout the late Quaternary, were not consistent with the hypothesis of a large river as a primary barrier responsible for the divergence of the two species. Instead, a scenario of isolation and divergence followed by geographic expansion and admixture as a consequence of Quaternary climatic oscillations was supported. Paleomodels also were not consistent with the idea that the hybrid zone originated in primary differentiation and favor a secondary contact scenario. Model fitting indicated that clines of different loci spanning the hybrid zone are coincident and concordant. The narrow cline for one Z-linked locus could be indicative of some form of post-zygotic selection hindering genetic homogenization between the two species.

Understanding population connectivity and genetic diversity is of fundamental importance to conservation. However, in globally threatened marine megafauna, challenges remain due to their elusive nature and wide-ranging distributions. As overexploitation continues to threaten biodiversity across the globe, such knowledge gaps compromise both the suitability and effectiveness of management actions. Here, we use a comparative framework to investigate genetic differentiation and diversity of manta rays, one of the most iconic yet vulnerable groups of elasmobranchs on the planet. Despite their recent divergence, we show how oceanic manta rays(Mobula birostris)display significantly higher genetic diversity than reef manta rays(Mobula alfredi)and thatM. birostrispopulations display higher connectivity worldwide. Through reconstructing modes of colonisation, we reveal how both contemporary and historical forces have likely influenced these patterns, with important implications for populatio...

Understanding the role of chromosomal inversions in speciation is a fundamental problem in evolutionary genetics. Here, we perform a comprehensive reconstruction of the evolutionary histories of the chromosomal inversions in Drosophila persimilis and D. pseudoobscura. We provide a solution to the puzzling origins of the selfish Sex-Ratio arrangement in D. persimilis and uncover surprising patterns of phylogenetic discordance on this chromosome. These patterns show that, contrary to widely held views, all fixed chromosomal inversions between D. persimilis and D. pseudoobscura were already present in their ancestral population long before the species split. Our results suggest that patterns of higher genomic divergence and an association of reproductive isolation genes with chromosomal inversions may be a direct consequence of incomplete lineage sorting of ancestral polymorphisms. These findings force a reconsideration of the role of chromosomal inversions in speciation, not as protectors of existing hybrid incompatibilities, but as fertile grounds for their formation.

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 s...

Background: Speciation with gene flow is an alternative to the nascence of new taxa in strict allopatric separation. Indeed, many taxa have parapatric distributions at present. It is often unclear if these are secondary contacts, e.g. caused by past glaciation cycles or the manifestation of speciation with gene flow, which hampers our understanding of how different forces drive diversification. Here we studied genetic, phenotypic and ecological aspects of divergence in a pair of incipient shorebird species, the Kentish (Charadrius alexandrinus) and the Whitefaced Plovers (C. dealbatus), shorebirds with parapatric breeding ranges along the Chinese coast. We assessed divergence based on molecular markers with different modes of inheritance and quantified phenotypic and ecological divergence in aspects of morphometric, dietary and climatic niches. Results: Our integrative analyses revealed small to moderate levels of genetic and phenotypic distinctiveness with symmetric gene flow across the contact area at the Chinese coast. The two species diverged approximately half a million years ago in dynamic isolation with secondary contact occurring due to cycling sea level changes between the Eastern and Southern China Sea in the mid-late Pleistocene. We found evidence of character displacement and ecological niche differentiation between the two species, invoking the role of selection in facilitating divergence despite gene flow. Conclusion: These findings imply that ecology can indeed counter gene flow through divergent selection and thus contributes to incipient speciation in these plovers. Furthermore, our study highlights the importance of using integrative datasets to reveal the evolutionary history and assist the inference of mechanisms of speciation.

The grain beetle, Oryzaephilus surinamensis, is a widespread species distributed in the wild and in granaries. Our earlier extensive biological studies indicated that the beetle shows incipient sympatric speciation (SS) in the wild at Evolution Canyon I (EC-I), Israel, and allopatric speciation, in a granary. Here we provide genome-wide evidence supporting our adaptive evolution scenario involving two models of speciation, SS in the wild, and allopatric in the granary. The EC-I microsite is a hot spot of SS across life from bacteria to mammals caused by the sharp opposite microclimates. The tropical hot, dry and savannoid biome dubbed the “African” slope (AS), sharply contrasts with the opposite temperate, cool, humid, and forested biome on the European” slope (ES), separated by only ~250 meters. The third allopatric granary population is 26 km north of EC-I. The granary population showed larger genomic, morphological, and behavioral distances, smaller genome size, more unique trans...