Evidence for nonallopatric speciation among closely related sympatric Heliotropium species in the Atacama Desert

The genetic structure of populations of closely related, sympatric species may hold the signature of the geographical mode of the speciation process. In fully allopatric speciation, it is expected that genetic differentiation between species is homogeneously distributed across the genome. In nonallopatric speciation, the genomes may remain undifferentiated to a large extent. In this article, we analyzed the genetic structure of five sympatric species from the plant genus Heliotropium in the Atacama Desert. We used amplified fragment length polymorphisms (AFLPs) to characterize the genetic structure of these species and evaluate their genetic differentiation as well as the number of loci subject to positive selection using divergence outlier analysis (DOA). The five species form distinguishable groups in the genetic space, with zones of overlap, indicating that they are possibly not completely isolated. Among‐species differentiation accounts for 35% of the total genetic differentiation (F_ST = 0.35), and F_ST between species pairs is positively correlated with phylogenetic distance. DOA suggests that few loci are subject to positive selection, which is in line with a scenario of nonallopatric speciation. These results support the idea that sympatric species of Heliotropium sect. Cochranea are under an ongoing speciation process, characterized by a fluctuation of population ranges in response to pulses of arid and humid periods during Quaternary times.     

Genomic footprints of speciation in Atlantic eels (Anguilla anguilla and A. rostrata)

The importance of speciation‐with‐geneflow scenarios is increasingly appreciated. However, the specific processes and the resulting genomic footprints of selection are subject to much discussion. We studied the genomics of speciation between the two panmictic, sympatrically spawning sister species; European (Anguilla anguilla) and American eel (A. rostrata). Divergence is assumed to have initiated more than 3 Ma, and although low gene flow still occurs, strong postzygotic barriers are present. Restriction‐site‐associated DNA (RAD) sequencing identified 328 300 SNPs for subsequent analysis. However, despite the presence of 3757 strongly differentiated SNPs (F_ST > 0.8), sliding window analyses of F_ST showed no larger genomic regions (i.e. hundreds of thousands to millions of bases) of elevated differentiation. Overall F_ST was 0.041, and linkage disequilibrium was virtually absent for SNPs separated by more than 1000 bp. We suggest this to reflect a case of genomic hitchhiking, where multiple regions are under directional selection between the species. However, low but biologically significant gene flow and high effective population sizes leading to very low genetic drift preclude accumulation of strong background differentiation. Genes containing candidate SNPs for positive selection showed significant enrichment for gene ontology (GO) terms relating to developmental processes and phosphorylation, which seems consistent with assumptions that differences in larval phase duration and migratory distances underlie speciation. Most SNPs under putative selection were found outside coding regions, lending support to emerging views that noncoding regions may be more functionally important than previously assumed. In total, the results demonstrate the necessity of interpreting genomic footprints of selection in the context of demographic parameters and life‐history features of the studied species.     

Exploring a Pool‐seq‐only approach for gaining population genomic insights in nonmodel species

Developing genomic insights is challenging in nonmodel species for which resources are often scarce and prohibitively costly. Here, we explore the potential of a recently established approach using Pool‐seq data to generate a de novo genome assembly for mining exons, upon which Pool‐seq data are used to estimate population divergence and diversity. We do this for two pairs of sympatric populations of brown trout (Salmo trutta): one naturally sympatric set of populations and another pair of populations introduced to a common environment. We validate our approach by comparing the results to those from markers previously used to describe the populations (allozymes and individual‐based single nucleotide polymorphisms [SNPs]) and from mapping the Pool‐seq data to a reference genome of the closely related Atlantic salmon (Salmo salar). We find that genomic differentiation (F_ST) between the two introduced populations exceeds that of the naturally sympatric populations (F_ST = 0.13 and 0.03 between the introduced and the naturally sympatric populations, respectively), in concordance with estimates from the previously used SNPs. The same level of population divergence is found for the two genome assemblies, but estimates of average nucleotide diversity differ ( ≈ 0.002 and  ≈ 0.001 when mapping to S. trutta and S. salar, respectively), although the relationships between population values are largely consistent. This discrepancy might be attributed to biases when mapping to a haploid condensed assembly made of highly fragmented read data compared to using a high‐quality reference assembly from a divergent species. We conclude that the Pool‐seq‐only approach can be suitable for detecting and quantifying genome‐wide population differentiation, and for comparing genomic diversity in populations of nonmodel species where reference genomes are lacking.     

The genomic bases of morphological divergence and reproductive isolation driven by ecological speciation in Senecio (Asteraceae)

Ecological speciation, driven by adaptation to contrasting environments, provides an attractive opportunity to study the formation of distinct species, and the role of selection and genomic divergence in this process. Here, we focus on a particularly clear‐cut case of ecological speciation to reveal the genomic bases of reproductive isolation and morphological differences between closely related Senecio species, whose recent divergence within the last ~200 000 years was likely driven by the uplift of Mt. Etna (Sicily). These species form a hybrid zone, yet remain morphologically and ecologically distinct, despite active gene exchange. Here, we report a high‐density genetic map of the Senecio genome and map hybrid breakdown to one large and several small quantitative trait loci (QTL). Loci under diversifying selection cluster in three 5 cM regions which are characterized by a significant increase in relative (F_ST), but not absolute (d_XY), interspecific differentiation. They also correspond to some of the regions of greatest marker density, possibly corresponding to ‘cold‐spots’ of recombination, such as centromeres or chromosomal inversions. Morphological QTL for leaf and floral traits overlap these clusters. We also detected three genomic regions with significant transmission ratio distortion (TRD), possibly indicating accumulation of intrinsic genetic incompatibilities between these recently diverged species. One of the TRD regions overlapped with a cluster of high species differentiation, and another overlaps the large QTL for hybrid breakdown, indicating that divergence of these species may have occurred due to a complex interplay of ecological divergence and accumulation of intrinsic genetic incompatibilities.     

Size differentiation in Finnish house sparrows follows Bergmann's rule with evidence of local adaptation

Bergmann's rule predicts that individuals are larger in more poleward populations and that this size gradient has an adaptive basis. Hence, phenotypic divergence in size traits between populations (P_ST) is expected to exceed the level of divergence by drift alone (F_ST). We measured 16 skeletal traits, body mass and wing length in 409 male and 296 female house sparrows Passer domesticus sampled in 12 populations throughout Finland, where the species has its northernmost European distributional margin. Morphometric differentiation across populations (P_ST) was compared with differentiation in 13 microsatellites (F_ST). We find that twelve traits phenotypically diverged more than F_ST in both sexes, and an additional two traits diverged in males. The phenotypic divergence exceeded F_ST in several traits to such a degree that findings were robust also to strong between‐population environmental effects. Divergence was particularly strong in dimensions of the bill, making it a strong candidate for the study of adaptive molecular genetic divergence. Divergent traits increased in size in more northern populations. We conclude that house sparrows show evidence of an adaptive latitudinal size gradient consistent with Bergmann's rule on the modest spatial scale of ca. 600 km.     

Genetic divergence between the sympatric queen morphs of the ant Myrmica rubra

Pairs of obligate social parasites and their hosts, where some of the parasites have recently diverged from their host through intraspecific social parasitism, provide intriguing systems for studying the modes and processes of speciation. Such speciation, probably in sympatry, has also been propounded in the ant Myrmica rubra and its intraspecific social parasite. In this species, parasitism is associated with queen size dimorphism, and the small microgyne has become a social parasite of the large macrogyne. Here, we investigated the genetic divergence of the host and the parasite queen morphs in 11 localities in southern Finland, using nuclear and mitochondrial markers of queens and workers. We formulated and tested four speciation‐related hypotheses that differed in the degree of genetic divergence between the morphs. The queen morphs were genetically distinct from each other with little hybridization. In the nuclear data, when localities were nested within queen morphs in the hierarchical amova , 39% of the genetic variation was explained by the queen morph (standardized F'_CT = 0.63, uncorrected F_CT = 0.39), whereas 18% was explained by the locality (F'_SC = 0.39, F_SC = 0.29). This result corroborated the hypothesis of advanced sympatric speciation. In contrast, the mitochondrial DNA could not settle between the hierarchical levels of locality and queen morph, thus substantiating equally the hypotheses of incipient and advanced sympatric speciation. Together, our results support the view that the microgynous parasite has genetically diverged from its macrogynous host to the level of a nascent species.     

Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes

Determining the genetic bases of adaptations and their roles in speciation is a prominent issue in evolutionary biology. Cichlid fish species flocks are a prime example of recent rapid radiations, often associated with adaptive phenotypic divergence from a common ancestor within a short period of time. In several radiations of freshwater fishes, divergence in ecomorphological traits — including body shape, colour, lips and jaws — is thought to underlie their ecological differentiation, specialization and, ultimately, speciation. The Midas cichlid species complex (Amphilophus spp.) of Nicaragua provides one of the few known examples of sympatric speciation where species have rapidly evolved different but parallel morphologies in young crater lakes. This study identified significant QTL for body shape using SNPs generated via ddRAD sequencing and geometric morphometric analyses of a cross between two ecologically and morphologically divergent, sympatric cichlid species endemic to crater Lake Apoyo: an elongated limnetic species (Amphilophus zaliosus) and a high‐bodied benthic species (Amphilophus astorquii). A total of 453 genome‐wide informative SNPs were identified in 240 F₂ hybrids. These markers were used to construct a genetic map in which 25 linkage groups were resolved. Seventy‐two segregating SNPs were linked to 11 QTL. By annotating the two most highly supported QTL‐linked genomic regions, genes that might contribute to divergence in body shape along the benthic–limnetic axis in Midas cichlid sympatric adaptive radiations were identified. These results suggest that few genomic regions of large effect contribute to early stage divergence in Midas cichlids.     

Speciation genomics and a role for the Z chromosome in the early stages of divergence between Mexican ducks and mallards

Speciation is a continuous and dynamic process, and studying organisms during the early stages of this process can aid in identifying speciation mechanisms. The mallard (Anas platyrhynchos) and Mexican duck (A. [p.] diazi) are two recently diverged taxa with a history of hybridization and controversial taxonomy. To understand their evolutionary history, we conducted genomic scans to characterize patterns of genetic diversity and divergence across the mitochondrial DNA (mtDNA) control region, 3523 autosomal loci and 172 Z‐linked sex chromosome loci. Between the two taxa, Z‐linked loci (Φ_ST = 0.088) were 5.2 times more differentiated than autosomal DNA (Φ_ST = 0.017) but comparable to mtDNA (Φ_ST = 0.092). This elevated Z differentiation deviated from neutral expectations inferred from simulated data that incorporated demographic history and differences in effective population sizes between marker types. Furthermore, 3% of Z‐linked loci, compared to <0.1% of autosomal loci, were detected as outlier loci under divergent selection with elevated relative (Φ_ST) and absolute (d_XY) estimates of divergence. In contrast, the ratio of Z‐linked and autosomal differentiation among the seven Mexican duck sampling locations was close to 1:1 (Φ_ST = 0.018 for both markers). We conclude that between mallards and Mexican ducks, divergence at autosomal markers is largely neutral, whereas greater divergence on the Z chromosome (or some portions thereof) is likely the product of selection that has been important in speciation. Our results contribute to a growing body of literature indicating elevated divergence on the Z chromosome and its likely importance in avian speciation.     

Genomic islands of divergence linked to ecotypic variation in sockeye salmon

Regions of the genome displaying elevated differentiation (genomic islands of divergence) are thought to play an important role in local adaptation, especially in populations experiencing high gene flow. However, the characteristics of these islands as well as the functional significance of genes located within them remain largely unknown. Here, we used data from thousands of SNPs aligned to a linkage map to investigate genomic islands of divergence in three ecotypes of sockeye salmon (Oncorhynchus nerka) from a single drainage in southwestern Alaska. We found ten islands displaying high differentiation among ecotypes. Conversely, neutral structure observed throughout the rest of the genome was low and not partitioned by ecotype. One island on linkage group So13 was particularly large and contained six SNPs with F_ST > 0.14 (average F_ST of neutral SNPs = 0.01). Functional annotation revealed that the peak of this island contained a nonsynonymous mutation in a gene involved in growth in other species (TULP4). The islands that we discovered were relatively small (80–402 Kb), loci found in islands did not show reduced levels of diversity, and loci in islands displayed slightly elevated linkage disequilibrium. These attributes suggest that the islands discovered here were likely generated by divergence hitchhiking; however, we cannot rule out the possibility that other mechanisms may have produced them. Our results suggest that islands of divergence serve an important role in local adaptation with gene flow and represent a significant advance towards understanding the genetic basis of ecotypic differentiation.     

Post‐glacial colonization routes coincide with a life‐history breakpoint along a latitudinal gradient

Although adaptive divergence along environmental gradients has repeatedly been demonstrated, the role of post‐glacial colonization routes in determining phenotypic variation along gradients has received little attention. Here, we used a hierarchical Q_ST–F_ST approach to separate the roles of adaptive and neutral processes in shaping phenotypic variation in moor frog (Rana arvalis) larval life histories along a 1,700 km latitudinal gradient across northern Europe. This species has colonized Scandinavia via two routes with a contact zone in northern Sweden. By using neutral SNP and common garden phenotypic data from 13 populations at two temperatures, we showed that most of the variation along the gradient occurred between the two colonizing lineages. We found little phenotypic divergence within the lineages; however, all phenotypic traits were strongly diverged between the southern and northern colonization routes, with higher growth and development rates and larger body size in the north. The Q_ST estimates between the colonization routes were four times higher than F_ST, indicating a prominent role for natural selection. Q_ST within the colonization routes did not generally differ from F_ST, but we found temperature‐dependent adaptive divergence close to the contact zone. These results indicate that lineage‐specific variation can account for much of the adaptive divergence along a latitudinal gradient.     

High levels of interspecific gene flow in an endemic cichlid fish adaptive radiation from an extreme lake environment

Studying recent adaptive radiations in isolated insular systems avoids complicating causal events and thus may offer clearer insight into mechanisms generating biological diversity. Here, we investigate evolutionary relationships and genomic differentiation within the recent radiation of Alcolapia cichlid fish that exhibit extensive phenotypic diversification, and which are confined to the extreme soda lakes Magadi and Natron in East Africa. We generated an extensive RAD data set of 96 individuals from multiple sampling sites and found evidence for genetic admixture between species within Lake Natron, with the highest levels of admixture between sympatric populations of the most recently diverged species. Despite considerable environmental separation, populations within Lake Natron do not exhibit isolation by distance, indicating panmixia within the lake, although individuals within lineages clustered by population in phylogenomic analysis. Our results indicate exceptionally low genetic differentiation across the radiation despite considerable phenotypic trophic variation, supporting previous findings from smaller data sets; however, with the increased power of densely sampled SNPs, we identify genomic peaks of differentiation (F_ST outliers) between Alcolapia species. While evidence of ongoing gene flow and interspecies hybridization in certain populations suggests that Alcolapia species are incompletely reproductively isolated, the identification of outlier SNPs under diversifying selection indicates the radiation is undergoing adaptive divergence.     

Investigating the extent of parallelism in morphological and genomic divergence among lake trout ecotypes in Lake Superior

Understanding the emergence of species through the process of ecological speciation is a central question in evolutionary biology which also has implications for conservation and management. Lake trout (Salvelinus namaycush) is renowned for the occurrence of different ecotypes linked to resource and habitat use throughout North America. We aimed to unravel the fine genetic structure of the four lake trout ecotypes in Lake Superior. A total of 486 individuals from four sites were genotyped at 6822 filtered SNPs using RADseq technology. Our results revealed different extent of morphological and genetic differentiation within the different sites. Overall, genetic differentiation was weak but significant and was on average three times higher between sites (mean F_ST = 0.016) than between ecotypes within sites (mean F_ST = 0.005) indicating higher level of gene flow or a more recent shared ancestor between ecotypes within each site than between populations of the same ecotype. Evidence of divergent selection was also found between ecotypes and/or in association with morphological variation. Outlier loci found in genes related to lipid metabolism and visual acuity were of particular interest in this context of ecotypic divergence. However, we did not find clear indication of parallelism at the genomic level, despite the presence of phenotypic parallelism among some ecotypes from different sampling sites. Overall, the occurrence of different levels of both genomic and phenotypic differentiation between ecotypes within each site with several differentiated loci linked to relevant biological functions supports the presence of a continuum of divergence in lake trout.     

Divergent and linked selection shape patterns of genomic differentiation between European and North American Atlantic salmon (Salmo salar)

As populations diverge many processes can shape genomic patterns of differentiation. Regions of high differentiation can arise due to divergent selection acting on selected loci, genetic hitchhiking of nearby loci, or through repeated selection against deleterious alleles (linked background selection); this divergence may then be further elevated in regions of reduced recombination. Atlantic salmon (Salmo salar) from Europe and North America diverged >600,000 years ago and despite some evidence of secondary contact, the majority of genetic data indicate substantial divergence between lineages. This deep divergence with potential gene flow provides an opportunity to investigate the role of different mechanisms that shape the genomic landscape during early speciation. Here, using 184,295 single nucleotide polymorphisms (SNPs) and 80 populations, we investigate the genomic landscape of differentiation across the Atlantic Ocean with a focus on highly differentiated regions and the processes shaping them. We found evidence of high (mean F_ST = 0.26) and heterogeneous genomic differentiation between continents. Genomic regions associated with high trans‐Atlantic differentiation ranged in size from single loci (SNPs) within important genes to large regions (1–3 Mbp ) on four chromosomes (Ssa06, Ssa13, Ssa16 and Ssa19). These regions showed signatures consistent with selection, including high linkage disequilibrium, despite no significant reduction in recombination. Genes and functional enrichment of processes associated with differentiated regions may highlight continental differences in ocean navigation and parasite resistance. Our results provide insight into potential mechanisms underlying differences between continents, and evidence of near‐fixed and potentially adaptive trans‐Atlantic differences concurrent with a background of high genome‐wide differentiation supports subspecies designation in Atlantic salmon.     

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small N_e (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high F_ST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high F_ST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small N_e in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.     

RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic

Genomic studies of invasive species can reveal both invasive pathways and functional differences underpinning patterns of colonization success. The European green crab (Carcinus maenas) was initially introduced to eastern North America nearly 200 years ago where it expanded northwards to eastern Nova Scotia. A subsequent invasion to Nova Scotia from a northern European source allowed further range expansion, providing a unique opportunity to study the invasion genomics of a species with multiple invasions. Here, we use restriction‐site‐associated DNA sequencing‐derived SNPs to explore fine‐scale genomewide differentiation between these two invasions. We identified 9137 loci from green crab sampled from 11 locations along eastern North America and compared spatial variation to mitochondrial COI sequence variation used previously to characterize these invasions. Overall spatial divergence among invasions was high (pairwise F_ST ~0.001 to 0.15) and spread across many loci, with a mean F_ST ~0.052 and 52% of loci examined characterized by F_ST values >0.05. The majority of the most divergent loci (i.e., outliers, ~1.2%) displayed latitudinal clines in allele frequency highlighting extensive genomic divergence among the invasions. Discriminant analysis of principal components (both neutral and outlier loci) clearly resolved the two invasions spatially and was highly correlated with mitochondrial divergence. Our results reveal extensive cryptic intraspecific genomic diversity associated with differing patterns of colonization success and demonstrates clear utility for genomic approaches to delineating the distribution and colonization success of aquatic invasive species.     

The shape of things to come in the study of the origin of species?

Perhaps Darwin would agree that speciation is no longer the mystery of mysteries that it used to be. It is now generally accepted that evolution by natural selection can contribute to ecological adaptation, resulting in the evolution of reproductive barriers and, hence, to the evolution of new species (Schluter & Conte 2009 ; Meyer 2011 ; Nosil 2012 ). From genes that encode silencing proteins that cause infertility in hybrid mice (Mihola et al. 2009 ), to segregation distorters linked to speciation in fruit flies (Phadnis & Orr 2009 ), or pollinator‐mediated selection on flower colour alleles driving reinforcement in Texan wildflowers (Hopkins & Rausher 2012 ), characterization of the genes that drive speciation is providing clues to the origin of species (Nosil & Schluter 2011 ). It is becoming apparent that, while recent work continues to overturn historical ideas about sympatric speciation (e.g. Barluenga et al. 2006 ), ecological circumstances strongly influence patterns of genomic divergence, and ultimately the establishment of reproductive isolation when gene flow is present (Elmer & Meyer 2011 ). Less clear, however, are the genetic mechanisms that cause speciation, particularly when ongoing gene flow is occurring. Now, in this issue, Franchini et al. ( 2014 ) employ a classic genetic mapping approach augmented with new genomic tools to elucidate the genomic architecture of ecologically divergent body shapes in a pair of sympatric crater lake cichlid fishes. From over 450 segregating SNPs in an F2 cross, 72 SNPs were linked to 11 QTL associated with external morphology measured by means of traditional and geometric morphometrics. Annotation of two highly supported QTL further pointed to genes that might contribute to ecological divergence in body shape in Midas cichlids, overall supporting the hypothesis that genomic regions of large phenotypic effect may be contributing to early‐stage divergence in Midas cichlids.     

Asynchronous spawning in sympatric populations of a hard coral reveals cryptic species and ancient genetic lineages

Genetic subdivision within a species is a vital component of the evolution of biodiversity. In some species of Acropora corals in Western Australia, conspecific individuals spawn in two seasons 6 months apart, which has the potential to impede gene flow and result in genetic divergence. Genetic comparison of sympatric spring and autumn spawners of Acropora samoensis was conducted to assess the level of reproductive isolation and genetic divergence between the spawning groups based on multiple loci (13 microsatellite loci, the mitochondrial control region and two nuclear introns). Bayesian clustering and principal coordinate analysis of the microsatellite loci showed a high level of genetic differentiation between the spawning groups (F’_ST = 0.30; P < 0.001), as did the sequence data from PaxC and Calmodulin (Φ_ST = 0.97 and 0.31, respectively). At the PaxC locus, the autumn and spring spawners were associated with two divergent lineages that were separated by an evolutionary distance of 1.7% and statistical tests indicate divergent selection in PaxC, suggesting this gene may play a role in coral spawning. This study indicates that the autumn and spring spawners represent two cryptic species, and highlights the importance of asynchronous spawning as a mechanism influencing speciation in corals.