Are sympatrically speciating Midas cichlid fish special? Patterns of morphological and genetic variation in the closely related species Archocentrus centrarchus

Established empirical cases of sympatric speciation are scarce, although there is an increasing consensus that sympatric speciation might be more common than previously thought. Midas cichlid fish are one of the few substantiated cases of sympatric speciation, and they formed repeated radiations in crater lakes. In contrast, in the same environment, such radiation patterns have not been observed in other species of cichlids and other families of fish. We analyze morphological and genetic variation in a cichlid species (Archocentrus centrarchus) that co‐inhabits several crater lakes with the Midas species complex. In particular, we analyze variation in body and pharyngeal jaw shape (two ecologically important traits in sympatrically divergent Midas cichlids) and relate that to genetic variation in mitochondrial control region and microsatellites. Using these four datasets, we analyze variation between and within two Nicaraguan lakes: a crater lake where multiple Midas cichlids have been described and a lake where the source population lives. We do not observe any within‐lake clustering consistent across morphological traits and genetic markers, suggesting the absence of sympatric divergence in A. centrarchus. Genetic differentiation between lakes was low and morphological divergence absent. Such morphological similarity between lakes is found not only in average morphology, but also when analyzing covariation between traits and degree of morphospace occupation. A combined analysis of the mitochondrial control region in A. centrarchus and Midas cichlids suggests that a difference between lineages in the timing of crater lake colonization cannot be invoked as an explanation for the difference in their levels of diversification. In light of our results, A. centrarchus represents the ideal candidate to study the genomic differences between these two lineages that might explain why some lineages are more likely to speciate and diverge in sympatry than others.     

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.     

Genomic signatures of divergent selection and speciation patterns in a ‘natural experiment’, the young parallel radiations of Nicaraguan crater lake cichlid fishes

Divergent selection is the main driving force in sympatric ecological speciation and may also play a strong role in divergence between allopatric populations. Characterizing the genome‐wide impact of divergent selection often constitutes a first step in unravelling the genetic bases underlying adaptation and ecological speciation. The Midas cichlid fish (Amphilophus citrinellus) species complex in Nicaragua is a powerful system for studying evolutionary processes. Independent colonizations of isolated young crater lakes by Midas cichlid populations from the older and great lakes of Nicaragua resulted in the repeated evolution of adaptive radiations by intralacustrine sympatric speciation. In this study we performed genome scans on two repeated radiations of crater lake species and their great lake source populations (1030 polymorphic AFLPs, n ～ 30 individuals per species). We detected regions under divergent selection (0.3% in the crater lake Xiloá flock and 1.7% in the older crater lake Apoyo radiation) that might be responsible for the sympatric diversifications. We find no evidence that the same genomic regions have been involved in the repeated evolution of parallel adaptations across crater lake flocks. However, there is some genetic parallelism apparent (seven out of 51 crater lake to great lake outlier loci are shared; 13.7%) that is associated with the allopatric divergence of both crater lake flocks. Interestingly, our results suggest that the number of outlier loci involved in sympatric and allopatric divergence increases over time. A phylogeny based on the AFLP data clearly supports the monophyly of both crater lake species flocks and indicates a parallel branching order with a primary split along the limnetic‐benthic axis in both radiations.     

Genomics of speciation and introgression in Princess cichlid fishes from Lake Tanganyika

How variation in the genome translates into biological diversity and new species originate has endured as the mystery of mysteries in evolutionary biology. African cichlid fishes are prime model systems to address speciation‐related questions for their remarkable taxonomic and phenotypic diversity, and the possible role of gene flow in this process. Here, we capitalize on genome sequencing and phylogenomic analyses to address the relative impacts of incomplete lineage sorting, introgression and hybrid speciation in the Neolamprologus savoryi‐complex (the ‘Princess cichlids’) from Lake Tanganyika. We present a time‐calibrated species tree based on whole‐genome sequences and provide strong evidence for incomplete lineage sorting in the early phases of diversification and multiple introgression events affecting different stages. Importantly, we find that the Neolamprologus chromosomes show centre‐to‐periphery biases in nucleotide diversity, sequence divergence, GC content, incomplete lineage sorting and rates of introgression, which are likely modulated by recombination density and linked selection. The detection of heterogeneous genomic landscapes has strong implications on the genomic mechanisms involved in speciation. Collinear chromosomal regions can be protected from gene flow and harbour incompatibility genes if they reside in lowly recombining regions, and coupling can evolve between nonphysically linked genomic regions (chromosome centres in particular). Simultaneously, higher recombination towards chromosome peripheries makes these more dynamic, evolvable regions where adaptation polymorphisms have a fertile ground. Hence, differences in genome architecture could explain the levels of taxonomic and phenotypic diversity seen in taxa with collinear genomes and might have contributed to the spectacular cichlid diversity observed today.     

THE GENETIC ARCHITECTURE OF REPRODUCTIVE ISOLATION DURING SPECIATION‐WITH‐GENE‐FLOW IN LAKE WHITEFISH SPECIES PAIRS ASSESSED BY RAD SEQUENCING

During speciation‐with‐gene‐flow, effective migration varies across the genome as a function of several factors, including proximity of selected loci, recombination rate, strength of selection, and number of selected loci. Genome scans may provide better empirical understanding of the genome‐wide patterns of genetic differentiation, especially if the variance due to the previously mentioned factors is partitioned. In North American lake whitefish (Coregonus clupeaformis), glacial lineages that diverged in allopatry about 60,000 years ago and came into contact 12,000 years ago have independently evolved in several lakes into two sympatric species pairs (a normal benthic and a dwarf limnetic). Variable degrees of reproductive isolation between species pairs across lakes offer a continuum of genetic and phenotypic divergence associated with adaptation to distinct ecological niches. To disentangle the complex array of genetically based barriers that locally reduce the effective migration rate between whitefish species pairs, we compared genome‐wide patterns of divergence across five lakes distributed along this divergence continuum. Using restriction site associated DNA (RAD) sequencing, we combined genetic mapping and population genetics approaches to identify genomic regions resistant to introgression and derive empirical measures of the barrier strength as a function of recombination distance. We found that the size of the genomic islands of differentiation was influenced by the joint effects of linkage disequilibrium maintained by selection on many loci, the strength of ecological niche divergence, as well as demographic characteristics unique to each lake. Partial parallelism in divergent genomic regions likely reflected the combined effects of polygenic adaptation from standing variation and independent changes in the genetic architecture of postzygotic isolation. This study illustrates how integrating genetic mapping and population genomics of multiple sympatric species pairs provide a window on the speciation‐with‐gene‐flow mechanism.     

Maintenance of species boundaries in a Neotropical radiation of Begonia

A major goal of evolutionary biology is to determine the mechanisms generating biodiversity. In Begonia, one of the largest plant genera (1900+ species), it has been postulated that the high number of endemic species is a by‐product of low gene flow among populations, which predisposes the group to speciation. However, this model of divergence requires that reproductive barriers accumulate rapidly among diverging species that overlap in their geographic ranges, otherwise speciation will be opposed by homogenizing gene flow in zones of secondary contact. Here, we test the outcomes of secondary contact in Begonia by genotyping multiple sympatric sites with 12 nuclear and seven plastid loci. We show that three sites of secondary contact between B. heracleifolia and B. nelumbiifolia are highly structured, mostly containing parental genotypes, with few F1 hybrids. A sympatric site between B. heracleifolia and B. sericoneura contains a higher proportion of F1s, but little evidence of introgression. The lack of later‐generation hybrids contrasts with that documented in many other plant taxa, where introgression is extensive. Our results, in conjunction with previous genetic work, show that Begonia demonstrate properties making them exceptionally prone to speciation, at multiple stages along the divergence continuum. Not only are populations weakly connected by gene flow, promoting allopatric speciation, but species often show strong reproductive barriers in secondary contact. Whether similar mechanisms contribute to diversification in other large genera remains to be tested.     

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.     

Genome divergence and diversification within a geographic mosaic of coevolution

Despite substantial interest in coevolution's role in diversification, examples of coevolution contributing to speciation have been elusive. Here, we build upon past studies that have shown both coevolution between South Hills crossbills and lodgepole pine (Pinus contorta), and high levels of reproductive isolation between South Hills crossbills and other ecotypes in the North American red crossbill (Loxia curvirostra) complex. We used genotyping by sequencing to generate population genomic data and applied phylogenetic and population genetic analyses to characterize the genetic structure within and among nine of the ecotypes. Although genome‐wide divergence was slight between ecotypes (F_ST = 0.011–0.035), we found evidence of relative genetic differentiation (as measured by F_ST) between and genetic cohesiveness within many of them. As expected for nomadic and opportunistic breeders, we detected no evidence of isolation by distance. The one sedentary ecotype, the South Hills crossbill, was genetically most distinct because of elevated divergence at a small number of loci rather than pronounced overall genome‐wide divergence. These findings suggest that mechanisms related to recent local coevolution between South Hills crossbills and lodgepole pine (e.g. strong resource‐based density dependence limiting gene flow) have been associated with genome divergence in the face of gene flow. Our results further characterize a striking example of coevolution driving speciation within perhaps as little as 6000 years.     

Untangling the evolutionary history of a highly polymorphic species: introgressive hybridization and high genetic structure in the desert cichlid fish Herichtys minckleyi

Understanding the origin of biodiversity requires knowledge on the evolutionary processes that drive divergence and speciation, as well as on the processes constraining it. Intraspecific polymorphisms can provide insight into the mechanisms that generate and maintain phenotypic, behavioural and life history diversification, and can help us understand not only the processes that lead to speciation but also the processes that prevent local fixation of morphs. The ‘desert cichlid’ Herichtys minckleyi is a highly polymorphic species endemic to a biodiversity hotspot in northern Mexico, the Cuatro Ciénegas valley. This species is polymorphic in body shape and trophic apparatus, and eco‐morphotypes coexist in small spring‐fed lagoons across the valley. We investigated the genetic structure of these polymorphisms and their phylogeographic history by analysing the entire control region of the mitochondrial DNA and 10 nuclear microsatellite markers in several populations from different sites and morphs. We found two very divergent mitochondrial lineages that most likely predate the closing of the valley and are not associated with morphotypes or sites. One of these lineages is also found in the sister species Herichthys cyanoguttatus. Data from neutral microsatellite markers suggest that most lagoons or drainages constitute their own genetic cluster with sympatric eco‐morphotypes forming panmictic populations. Alternative mechanisms such as phenotypic plasticity and a few loci controlled traits provide possible explanations for the sympatric coexistence of discrete nonoverlapping eco‐morphotypes with apparent lack of barriers to gene flow within multiple lagoons and drainages.     

The puzzling phylogeography of the haplochromine cichlid fish Astatotilapia burtoni

Astatotilapia burtoni is a member of the “modern haplochromines,” the most species‐rich lineage within the family of cichlid fishes. Although the species has been in use as research model in various fields of research since almost seven decades, including developmental biology, neurobiology, genetics and genomics, and behavioral biology, little is known about its spatial distribution and phylogeography. Here, we examine the population structure and phylogeographic history of A. burtoni throughout its entire distribution range in the Lake Tanganyika basin. In addition, we include several A. burtoni laboratory strains to trace back their origin from wild populations. To this end, we reconstruct phylogenetic relationships based on sequences of the mitochondrial DNA (mtDNA) control region (d‐loop) as well as thousands of genomewide single nucleotide polymorphisms (SNPs) derived from restriction‐associated DNA sequencing. Our analyses reveal high population structure and deep divergence among several lineages, however, with discordant nuclear and mtDNA phylogenetic inferences. Whereas the SNP‐based phylogenetic hypothesis uncovers an unexpectedly deep split in A. burtoni, separating the populations in the southern part of the Lake Tanganyika basin from those in the northern part, analyses of the mtDNA control region suggest deep divergence between populations from the southwestern shoreline and populations from the northern and southeastern shorelines of Lake Tanganyika. This phylogeographic pattern and mitochondrial haplotype sharing between populations from the very North and the very South of Lake Tanganyika can only partly be explained by introgression linked to lake‐level fluctuations leading to past contact zones between otherwise isolated populations and large‐scale migration events.     

Divergent parasite infections in sympatric cichlid species in Lake Victoria

Parasitism has been proposed as a factor in host speciation, as an agent affecting coexistence of host species in species‐rich communities and as a driver of post‐speciation diversification. Young adaptive radiations of closely related host species of varying ecological and genomic differentiation provide interesting opportunities to explore interactions between patterns of parasitism, divergence and coexistence of sympatric host species. Here, we explored patterns in ectoparasitism in a community of 16 fully sympatric cichlid species at Makobe Island in Lake Victoria, a model system of vertebrate adaptive radiation. We asked whether host niche, host abundance or host genetic differentiation explains variation in infection patterns. We found significant differences in infections, the magnitude of which was weakly correlated with the extent of genomic divergence between the host species, but more strongly with the main ecological gradient, water depth. These effects were most evident with infections of Cichlidogyrus monogeneans, whereas the only host species with a strictly crevice‐dwelling niche, Pundamilia pundamilia, deviated from the general negative relationship between depth and parasitism. In accordance with the Janzen–Connell hypothesis, we also found that host abundance tended to be positively associated with infections in some parasite taxa. Data on the Pundamilia sister species pairs from three other islands with variable degrees of habitat (crevice) specialization suggested that the lower parasite abundance of P. pundamilia at Makobe could result from both habitat specialization and the evolution of specific resistance. Our results support influences of host genetic differentiation and host ecology in determining infections in this diverse community of sympatric cichlid species.     

Genetic mapping of horizontal stripes in Lake Victoria cichlid fishes: benefits and pitfalls of using RAD markers for dense linkage mapping

The genetic dissection of naturally occurring phenotypes sheds light on many fundamental and longstanding questions in speciation and adaptation and is a central research topic in evolutionary biology. Until recently, forward‐genetic approaches were virtually impossible to apply to nonmodel organisms, but the development of next‐generation sequencing techniques eases this difficulty. Here, we use the ddRAD‐seq method to map a colour trait with a known adaptive function in cichlid fishes, well‐known textbook examples for rapid rates of speciation and astonishing phenotypic diversification. A suite of phenotypic key innovations is related to speciation and adaptation in cichlids, among which body coloration features prominently. The focal trait of this study, horizontal stripes, evolved in parallel in several cichlid radiations and is associated with piscivorous foraging behaviour. We conducted interspecific crosses between Haplochromis sauvagei and H. nyererei and constructed a linkage map with 867 SNP markers distributed on 22 linkage groups and total size of 1130.63 cM. Lateral stripes are inherited as a Mendelian trait and map to a single genomic interval that harbours a paralog of a gene with known function in stripe patterning. Dorsolateral and mid‐lateral stripes were always coinherited and are thus under the same genetic control. Additionally, we directly quantify the genotyping error rates in RAD markers and offer guidelines for identifying and dealing with errors. Uncritical marker selection was found to severely impact linkage map construction. Fortunately, by applying appropriate quality control steps, a genotyping accuracy of >99.9% can be reached, thus allowing for efficient linkage mapping of evolutionarily relevant traits.     

Introgression and selection shaped the evolutionary history of sympatric sister‐species of coral reef fishes (genus: Haemulon)

Closely related marine species with large overlapping ranges provide opportunities to study mechanisms of speciation, particularly when there is evidence of gene flow between such lineages. Here, we focus on a case of hybridization between the sympatric sister‐species Haemulon maculicauda and H. flaviguttatum, using Sanger sequencing of mitochondrial and nuclear loci, as well as 2422 single nucleotide polymorphisms (SNPs) obtained via restriction site‐associated DNA sequencing (RADSeq). Mitochondrial markers revealed a shared haplotype for COI and low divergence for CytB and CR between the sister‐species. On the other hand, complete lineage sorting was observed at the nuclear loci and most of the SNPs. Under neutral expectations, the smaller effective population size of mtDNA should lead to fixation of mutations faster than nDNA. Thus, these results suggest that hybridization in the recent past (0.174–0.263 Ma) led to introgression of the mtDNA, with little effect on the nuclear genome. Analyses of the SNP data revealed 28 loci potentially under divergent selection between the two species. The combination of mtDNA introgression and limited nuclear DNA introgression provides a mechanism for the evolution of independent lineages despite recurrent hybridization events. This study adds to the growing body of research that exemplifies how genetic divergence can be maintained in the presence of gene flow between closely related species.     

Recent speciation between sympatric Tanganyikan cichlid colour morphs

Lake Tanganyika, Africa's oldest lake, harbours an impressive diversity of cichlid fishes. Although diversification in its radiating groups is thought to have been initially rapid, cichlids from Lake Tanganyika show little evidence for ongoing speciation. In contrast, examples of recent divergence among sympatric colour morphs are well known in haplochromine cichlids from Lakes Malawi and Victoria. Here, we report genetic evidence for recent divergence between two sympatric Tanganyikan cichlid colour morphs. These Petrochromis morphs share mitochondrial haplotypes, yet microsatellite loci reveal that their sympatric populations form distinct genetic groups. Nuclear divergence between the two morphs is equivalent to that which arises geographically within one of the morphs over short distances and is substantially smaller than that among other sympatric species in this genus. These patterns suggest that these morphs diverged only recently, yet that barriers to gene flow exist which prevent extensive admixture despite their sympatric distribution. The morphs studied here provide an unusual example of active diversification in Lake Tanganyika's generally ancient cichlid fauna and enable comparisons of speciation processes between Lake Tanganyika and other African lakes.     

A test of genomic modularity among life‐history adaptations promoting speciation with gene flow

Speciation with gene flow may require adaptive divergence of multiple traits to generate strong ecologically based reproductive isolation. Extensive negative pleiotropy or physical linkage of genes in the wrong phase affecting these diverging traits may therefore hinder speciation, while genetic independence or “modularity” among phenotypic traits may reduce constraints and facilitate divergence. Here, we test whether the genetics underlying two components of diapause life history, initial diapause intensity and diapause termination timing, constrain differentiation between sympatric hawthorn and apple‐infesting host races of the fly Rhagoletis pomonella through analysis of 10,256 SNPs measured via genotyping‐by‐sequencing (GBS). Loci genetically associated with diapause termination timing were mainly observed for SNPs mapping to chromosomes 1–3 in the genome, most notably for SNPs displaying higher levels of linkage disequilibrium (LD), likely due to inversions. In contrast, selection on initial diapause intensity affected loci on all five major chromosomes of the genome, specifically those showing low levels of LD. This lack of overlap in genetically associated loci suggests that the two diapause phenotypes are largely modular. On chromosome 2, however, intermediate level LD loci and a subgroup of high LD loci displayed significant negative relationships between initial diapause intensity and diapause termination time. These gene regions on chromosome 2 therefore affected both traits, while most regions were largely independent. Moreover, loci associated with both measured traits also tended to exhibit highly divergent allele frequencies between the host races. Thus, the presence of nonoverlapping genetic modules likely facilitates simultaneous, adaptive divergence for the measured life‐history components.     

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.     

Model‐based demographic inference of introgression history in European whitefish species pairs'

Parallel phenotypic differentiation is generally attributed to parallel adaptive divergence as an evolutionary response to similar environmental contrasts. Such parallelism may actually originate from several evolutionary scenarios ranging from repeated parallel divergence caused by divergent selection to a unique divergence event followed by gene flow. Reconstructing the evolutionary history underlying parallel phenotypic differentiation is thus fundamental to understand the relative contribution of demography and selection on genomic divergence during speciation. In this study, we investigate the divergence history of replicate European whitefish (Coregonus lavaretus), limnetic and benthic species pairs from two lakes in Norway and two lakes in Switzerland. Demographic models accounting for semi‐permeability and linked selection were fitted to the unfolded joint allele frequency spectrum built from genome‐wide SNPs and compared to each other in each species pair. We found strong support for a model of asymmetrical post‐glacial secondary contact between glacial lineages in all four lakes. Moreover, our results suggest that heterogeneous genomic differentiation has been shaped by the joint action of linked selection accelerating lineage sorting during allopatry, and heterogeneous migration eroding divergence at different rates along the genome following secondary contact. Our analyses reveal how the interplay between demography, selection and historical contingency has influenced the levels of diversity observed in previous whitefish phylogeographic studies. This study thus provides new insights into the historical demographic and selective processes that shaped the divergence associated with ecological speciation in European whitefish.     

Complex histories of repeated gene flow in Cameroon crater lake cichlids cast doubt on one of the clearest examples of sympatric speciation

One of the most celebrated examples of sympatric speciation in nature are monophyletic radiations of cichlid fishes endemic to Cameroon crater lakes. However, phylogenetic inference of monophyly may not detect complex colonization histories involving some allopatric isolation, such as double invasions obscured by genome‐wide gene flow. Population genomic approaches are better suited to test hypotheses of sympatric speciation in these cases. Here, we use comprehensive sampling from all four sympatric crater lake cichlid radiations in Cameroon and outgroups across Africa combined with next‐generation sequencing to genotype tens of thousands of SNPs. We find considerable evidence of gene flow between all four radiations and neighboring riverine populations after initial colonization. In a few cases, some sympatric species are more closely related to outgroups than others, consistent with secondary gene flow facilitating their speciation. Our results do not rule out sympatric speciation in Cameroon cichlids, but rather reveal a complex history of speciation with gene flow, including allopatric and sympatric phases, resulting in both reproductively isolated species and incipient species complexes. The best remaining non‐cichlid examples of sympatric speciation all involve assortative mating within microhabitats. We speculate that this feature may be necessary to complete the process of sympatric speciation in nature.     

Differential divergence in autosomes and sex chromosomes is associated with intra‐island diversification at a very small spatial scale in a songbird lineage

Recently diverged taxa showing marked phenotypic and ecological diversity provide optimal systems to understand the genetic processes underlying speciation. We used genome‐wide markers to investigate the diversification of the Reunion grey white‐eye (Zosterops borbonicus) on the small volcanic island of Reunion (Mascarene archipelago), where this species complex exhibits four geographical forms that are parapatrically distributed across the island and differ strikingly in plumage colour. One form restricted to the highlands is separated by a steep ecological gradient from three distinct lowland forms which meet at narrow hybrid zones that are not associated with environmental variables. Analyses of genomic variation based on single nucleotide polymorphism data from genotyping‐by‐sequencing and pooled RAD‐seq approaches show that signatures of selection associated with elevation can be found at multiple regions across the genome, whereas most loci associated with the lowland forms are located on the Z sex chromosome. We identified TYRP1, a Z‐linked colour gene, as a likely candidate locus underlying colour variation among lowland forms. Tests of demographic models revealed that highland and lowland forms diverged in the presence of gene flow, and divergence has progressed as gene flow was restricted by selection at loci across the genome. This system holds promise for investigating how adaptation and reproductive isolation shape the genomic landscape of divergence at multiple stages of the speciation process.