Ancient lakes revisited: from the ecology to the genetics of speciation

Explosive speciation in ancient lakes has fascinated biologists for centuries and has inspired classical work on the tempo and modes of speciation. Considerable attention has been directed towards the extrinsic forces of speciation—the geological, geographical and ecological peculiarities of ancient lakes. Recently, there has been a resurgence of interest in the intrinsic nature of these radiations, the biological characteristics conducive to speciation. While new species are thought to arise mainly by the gradual enhancement of reproductive isolation among geographically isolated populations, ancient lakes provide little evidence for a predominant role of geography in speciation. Recent phylogenetic work provides strong evidence that multiple colonization waves were followed by parallel intralacustrine radiations that proceeded at relatively rapid rates despite long‐term gene flow through hybridization and introgression. Several studies suggest that hybridization itself might act as a key evolutionary mechanism by triggering major genomic reorganization/revolution and enabling the colonization of new ecological niches in ancient lakes. These studies propose that hybridization is not only of little impediment to diversification but could act as an important force in facilitating habitat transitions, promoting postcolonization adaptations and accelerating diversification. Emerging ecological genomic approaches are beginning to shed light on the long‐standing evolutionary dilemma of speciation in the face of gene flow. We propose an integrative programme for future studies on speciation in ancient lakes.     

The ancient lakes of Indonesia: towards integrated research on speciation

Ancient lakes have provided considerable insights into the drivers of speciation and adaptive radiation in aquatic organisms. Most studies of species-flocks, however, focus only on a single group of organisms, and few have attempted to integrate geological, limnological, ecological, and genetic drivers of speciation on multiple species-flocks at various trophic levels. As such, there is a need for a comprehensive model system for research on speciation in aquatic environments where multiple radiations are investigated at various levels of biological organization (e.g., individual, population, and ecosystem) and placed in light of geographical and geological setting. The ancient Malili Lakes of Sulawesi, Indonesia, are ideal candidates for such a model, and represent the only hydrologically connected ancient lakes in the world. These lakes are characterized by ultra-oligotrophy and unique physicochemical conditions that govern the composition and production of planktonic communities. At higher trophic levels, there are three recurring trends: (1) low taxonomic richness and simple community structures, (2) adaptive radiations with trophic specialization, and (3) remarkably high endemism with evolutionary innovations throughout the lakes and species-flocks. Furthermore, the restricted geographic distributions of species-flocks within the Malili Lakes indicate that each lake constitutes a unique environment, and dispersal among lakes is limited, despite close contemporary connectivity. These observations suggest that ecological and evolutionary processes are regulated from the bottom up, and speciation is primarily facilitated by interspecific and intraspecific competition for limited resources. The Malili Lakes represent an outstanding natural model for integrative research into speciation as they offer the opportunity to explore the roles of geography, dispersal, and selection in the radiation of aquatic organisms.     

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.     

Adaptive, pre-adaptive and non-adaptive components of radiations in ancient lakes: a review

Ancient lakes are ideal model systems for evolutionary studies, as they hold hundreds of endemic species. The vast majority of these still occur in the cradle of their origin. We distinguish three different modes of speciation (allo-, para- and sympatric) which have occurred in these habitats. Although radiations from ancient lakes are generally assumed to be adaptive, we cannot fully support this point of view, because non-adaptive radiations also appear to be common, for example through chromosomal changes, hybridization or sexual selection. Even in supposedly adaptive cladogenesis, e.g. as concerns the presumed trophic adaptations of cichlid (Pisces) mouth and tooth shapes, both adaptive and non-adaptive components are acting. Distribution patterns of non-marine ostracods (Crustacea) within and outside of ancient lakes indicate that sexual reproduction might be an additional requirement for successful radiations in ancient lakes, at least in certain groups. This can best be understood by invoking ecology-based hypotheses on the evolutionary superiority of sexual reproduction such as Fisher–Muller accelerated evolution and the Tangled Bank.     

African cichlid fish: a model system in adaptive radiation research

The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.     

Role of ancient lakes in genetic and phenotypic diversification of freshwater snails

Endemic organisms of ancient lakes have been studied as models to understand processes of speciation and adaptive radiation. However, it remains unclear how ancient lakes play roles in genetic and phenotypic diversity of freshwater mollusks. In the present study, we focus on viviparid freshwater snails in the ancient lakes of East and Southeast Asia (Japan and China) to address this question. Using molecular phylogenetic analyses based on mitochondrial (COI, 16S) and nuclear genes (18S, 28S, H3), we show that patterns of species diversification in viviparid lineages. Colonization to ancient lakes occurred independently in China and Japan at least four times, with subsequent diversification into more than two species within each lake group. Morphological analyses of fossil related viviparids suggest parallel phenotypic evolution occurred in the different lakes and ages. Each lake contained a single lineage which was phenotypically diversified relative to those from other sites. Using genome‐wide SNPs obtained by MIG‐seq, we also examined the genetic structure of three Japanese viviparids, including two endemic species of ancient Lake Biwa. The results suggest that these two species diversified from the population of the third species living in wetlands surrounding the lake. These findings suggest that rapid diversification of lineages and phenotypic divergence can occur in ancient lakes compared to other habitats. Formation of large lakes probably promotes speciation and phenotypic divergence as a result of adaptation into different microhabitats. High numbers of ancient lakes could be a driver of species diversity in Asian viviparid snails.     

Testing two contrasting evolutionary patterns in ancient lakes: species flock versus species scatter in valvatid gastropods of Lake Ohrid

Ancient lakes have long been recognized as “hot spots of evolution” and “evolutionary theatres” and they have significantly contributed to a better understanding of speciation and radiation processes in space and time. Yet, phylogenetic relationships of many ancient lake taxa, particularly invertebrate groups, are still unresolved. Also, the lack of robust morphological, anatomical, and phylogeographical data has largely prevented a rigorous testing of evolutionary hypotheses. For the freshwater gastropod genus Valvata—a group with a high degree of endemism in several ancient lakes—different evolutionary scenarios are suggested for different ancient lakes. Lake Baikal, for example, is inhabited by several endemic Valvata taxa that presumably do not form a monophyletic group. For such an evolutionary pattern, the term ancient lake species scatter is introduced here. In contrast, for the Balkan Lake Ohrid, workers previously suggested the presence of a monophyletic group of endemic Valvata species, that is, an ancient lake species flock. Sequence data of the mitochondrial cytochrome oxidase c subunit I gene (COI) from worldwide taxa, with a strong emphasis on Balkan species, are here used to test whether the putative Ohrid Valvata endemics represent an ancient lake species flock and to study patterns of speciation both on the Ohrid and the Balkan scale. The study reveals three distinct clades of endemic Valvata in Lake Ohrid. Monophyly of these taxa, however, is rejected, and they therefore do not represent an ancient lake species flock, but rather an ancient lake species scatter. Also, in contrast to many other gastropod groups in Lake Ohrid, the valvatids apparently did not radiate. Many Valvata taxa in ancient lakes are characterized by enhanced levels of shell complexity. However, it remains unclear whether these patterns are associated with ancient lake environments per se. It is here suggested that similarities in shell structure between North American and Balkan taxa might simply be due to convergent evolution.     

The species flocks of lacustrine gastropods: <Emphasis Type="Italic">Tylomelania</Emphasis> on Sulawesi as models in speciation and adaptive radiation

Endemic radiations provide splendid opportunities for studies in evolutionary biology. Species flocks in ancient lakes, such as in Tanganyika, Malawi or Baikal, have featured prominently in evolutionary biology, viewing these “evolutionary theatres” as hotspots of diversification. However, following a century of neglect, the endemic evolution of limnic cerithioidean gastropods in the two central lake systems on the Indonesian island of Sulawesi (i.e. Lake Poso and the lakes of the Malili system, e.g. Danau Matano, Mahalona and Towuti) also provide instructive model cases for the study of speciation mechanisms, adaptive radiation and annidation (i.e. niche exploitation). We here discuss the evolutionary and taxonomic implications of the lacustrine species flocks in Tylomelania from these lakes in Sulawesi as an exceptional endemic assemblage of morphologically distinct viviparous pachychilid gastropods. This first comprehensive compilation of data on both ancient lake systems, Poso and Malili, offers a new perspective on ecological differentiation in this radiation. Presented here within the framework of the theory of evolutionary ecology it provides a research program for acquiring a synthetical perspective that includes morphology, molecular genetics, ecology and biogeography. In this context, it will be possible to compare the species flocks of these truly “Darwinian snails” on Sulawesi with the long enigmatic, so-called thalassoid (i.e. marine-like) gastropod radiation in East African’s Lake Tanganyika.     

Molecular evidence reveals a polyphyletic origin and chromosomal speciation of Lake Baikal's endemic asellid isopods

The six endemic isopod species of Lake Baikal have been regarded as a small species flock with uncertain affinities to related asellids. We provide evidence from 16S rRNA sequences for polyphyletic origins of Baikalian Asellidae. One clade of two species is related to the Eurasian genus Asellus. The other clade, Baicalasellus, shows affinities to North American asellids and may have a long evolutionary history within the lake basin. Some speciation events within Baicalasellus clearly have a chromosomal basis. In contrast with numerous taxa exhibiting monophyletic radiations in ancient lakes, the endemic Baikalian isopods arose by multiple invasions and chromosomal mechanisms.     

Speciation in ancient lakes

About a dozen lakes in the world are up to three orders of magnitude older than most others. Lakes Tanganyika (East Africa) and Baikal (Siberia) have probably existed in some form for 12-20 million years, maybe more. Such lakes can have different origins, sizes, shapes, depths and limnologies, but, in contrast to short-lived (mostly post-glacial) lakes, they have exceptionally high faunal diversity and levels of endemicity. A multitude of and processes accounting for these explosive radiations have recently been documented, most of them based on particular groups in certain lakes, but comparative research can detect repeated patterns. No special speciafion mechanism, exclusive to ancient lakes has been demonstrated, although cases of ultra-rapid speciation have been documented. Extant diversity results not by simple accumulation, but by a complex process of immigration, speciation and extinction.     

Speciation patterns and processes in the zooplankton of the ancient lakes of Sulawesi Island,Indonesia

Although studies of ancient lake fauna have provided important insights about speciation patterns and processes of organisms in heterogeneous benthic environments, evolutionary forces responsible for speciation in the relatively homogenous planktonic environment remain largely unexplored. In this study, we investigate possible mechanisms of speciation in zooplankton using the freshwater diaptomids of the ancient lakes of Sulawesi, Indonesia, as a model system. We integrate phylogenetic and population genetic analyses of mitochondrial and nuclear genes with morphological and genome size data. Overall, our results support the conclusion that colonization order and local adaptation are dominant at the large, island scale, whereas at local and intralacustrine scales, speciation processes are regulated by gene flow among genetically differentiated and locally adapted populations. In the Malili lakes, the diaptomid populations are homogenous at nuclear loci, but show two highly divergent mitochondrial clades that are geographically restricted to single lakes despite the interconnectivity of the lake systems. Our study, based on coalescent simulations and population genetic analyses, indicates that unidirectional hybridization allows gene flow across the nuclear genome, but prevents the introgression of mitochondria into downstream populations. We suggest that hybridization and introgression between young lineages is a significant evolutionary force in freshwater plankton.     

Diversification rates have no effect on the convergent evolution of foraging strategies in the most speciose genus of bats,Myotis*

Adaptive radiations are defined as rapid diversification with phenotypic innovation led by colonization to new environments. Notably, adaptive radiations can occur in parallel when habitats with similar selective pressures are accessible promoting convergent adaptions. Although convergent evolution appears to be a common process, it is unclear what are the main drivers leading the reappearance of morphologies or ecological roles. We explore this question in Myotis bats, the only Chiropteran genus with a worldwide distribution. Three foraging strategies—gleaning, trawling, and aerial netting—repeatedly evolved in several regions of the world, each linked to characteristic morphologies recognized as ecomorphs. Phylogenomic, morphometric, and comparative approaches were adopted to investigate convergence of such foraging strategies and skull morphology as well as factors that explain diversification rates. Genomic and morphometric data were analyzed from ～80% extant taxa. Results confirm that the ecomorphs evolved multiple times, with trawling evolving more often and foliage gleaning most recently. Skull morphology does not reflect common ancestry and evolves convergently with foraging strategy. Although diversification rates have been roughly constant across the genus, speciation rates are area‐dependent and higher in taxa with temperate distributions. Results suggest that in this species‐rich group of bats, first, stochastic processes have led divergence into multiple lineages. Then, natural selection in similar niches has promoted repeated adaptation of phenotypes and foraging strategies. Myotis bats are thus a remarkable case of ecomorphological convergence and an emerging model system for investigating the genomic basis of parallel adaptive radiation.     

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.     

Partial island submergence and speciation in an adaptive radiation: a multilocus analysis of the Cuban green anoles

Sympatric speciation is often proposed to account for species-rich adaptive radiations within lakes or islands, where barriers to gene flow or dispersal may be lacking. However, allopatric speciation may also occur in such situations, especially when ranges are fragmented by fluctuating water levels. We test the hypothesis that Miocene fragmentation of Cuba into three palaeo-archipelagos accompanied species-level divergence in the adaptive radiation of West Indian Anolis lizards. Analysis of morphology, mitochondrial DNA (mt DNA) and nuclear DNA in the Cuban green anoles (carolinensis subgroup) strongly supports three pre dictions made by this hypothesis. First, three geographical sets of populations, whose ranges correspond with palaeo-archipelago boundaries, are distinct and warrant recognition as independent evolutionary lineages or species. Coalescence of nuclear sequence fragments sampled from these species and the large divergences observed between their mtDNA haplotypes suggest separation prior to the subsequent unification of Cuba ca. 5 Myr ago. Second, molecular phylogenetic relationships among these species reflect historical geographical relationships rather than morphological similarity. Third, all three species remain distinct despite extensive geographical contact subsequent to island unification, occasional hybridization and introgression of mtDNA haplotypes. Allopatric speciation initiated during partial island submergence may play an important role in speciation during the adaptive radiation of Anolis lizards.     

Rapid miocene-pliocene dispersal and evolution of Mediterranean rajid fauna as inferred by mitochondrial gene variation

Rajidae (colloquially known as skates and rays) experienced multiple and parallel adaptive radiations allowing high species diversity and great differences of species composition between regional faunas. Nevertheless, they show considerable conservation of bio-ecological, morphological and reproductive traits. The evolutionary history and dispersal of North-east Atlantic and Mediterranean rajid fauna were investigated throughout the sequence analysis of the control region and 16S rDNA mitochondrial genes. Molecular estimates of divergence times indicated recent origin and rapid dispersal of the present species. Compared with the ancient origin of the family (Late Cretaceous), the present species diversity arose in a relatively narrow time-window (12 Myr) from Middle Miocene to Early Pleistocene, likely by speciation processes related to dramatic geological and climatic events in the Mediterranean. Nucleotide substitution rates and phylogenetic relationships indicated Mediterranean endemic skates derived from sister species with wider distribution during Late Pliocene-Pleistocene. Skate phylogeny and systematics obtained using mitochondrial gene variation were largely consistent with those based on morpho-anatomical data.     

Rapid evolution of an ancient lake species flock: Freshwater limpets (Gastropoda: Ancylidae) in the Balkan Lake Ohrid

Ancient lakes have long been recognized as evolutionary theatres and hot spots of endemism; the evolution of their morphologically often highly diverse species flocks has received much attention. However, as each ancient lake has its own geological and evolutionary history, modes of speciation may differ from system to system. Ancient lakes can act as evolutionary reservoirs that assure the survival of relict species, but at the same time extant species may evolve through intralacustrine speciation. Other aspects of interest are the actual rates of immigration, diversification or extinction as well as the temporal framework of morphological change. Many of these questions have been addressed in the African (e.g. Lake Tanganyika) and Asian (e.g. Lake Baikal) ancient lakes. For an European ancient lakes (e.g. Lakes Ohrid and Prespa), such studies are largely missing. In the present paper, extraordinarily shaped endemic freshwater limpets of the genus Ancylus from the Balkan Lake Ohrid are used in a phylogeographic and phylogenetic context to test whether they represent an ancient lake species flock, to study the mode of speciation, and to assess the timing of morphological change. Based on DNA data from two mitochondrial genes (COI, LSU rDNA), it has been found that the Lake Ohrid Ancylus species form an endemic monophyletic group. In addition, the lake's feeder springs are inhabited by another, undescribed Ancylus species. All other studied waterbodies within the watershed do not support their own Ancylus lineages but are inhabited by a widespread Mediterranean taxon. The split between the species endemic to the lake and its sister taxon is dated to 1.4±0.6 million years ago. The study presents the first genetic confirmation for the existence of a species flock in a European ancient lake. Contrary to the prevailing opinion it shows that, concerning Ancylus, Lake Ohrid represents a site of intralacustrine speciation rather than an evolutionary reservoir. Moreover, it provides the first evidence for rapid morphological change in an European ancient lake species flock. See also Electronic Supplement at: http://www.senckenberg.de/odes/06-12.htm.     

Rapid parallel adaptive radiations from a single hybridogenic ancestral population

The Alpine lake whitefish (Coregonus lavaretus) species complex is a classic example of a recent radiation, associated with colonization of the Alpine lakes following the glacial retreat (less than 15 kyr BP). They have formed a unique array of endemic lake flocks, each with one to six described sympatric species differing in morphology, diet and reproductive ecology. Here, we present a genomic investigation of the relationships between and within the lake flocks. Comparing the signal between over 1000 AFLP loci and mitochondrial control region sequence data, we use phylogenetic tree-based and population genetic methods to reconstruct the phylogenetic history of the group and to delineate the principal centres of genetic diversity within the radiation. We find significant cytonuclear discordance showing that the genomically monophyletic Alpine whitefish clade arose from a hybrid swarm of at least two glacial refugial lineages. Within this radiation, we find seven extant genetic clusters centred on seven lake systems. Most interestingly, we find evidence of sympatric speciation within and parallel evolution of equivalent phenotypes among these lake systems. However, we also find the genetic signature of human-mediated gene flow and diversity loss within many lakes, highlighting the fragility of recent radiations.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

Gradual speciation in a global hotspot of plant diversity

The speciation process that underlies recent, rapid radiations of plants is controversial, and suggested mechanisms range from pollinator or ecological niche differentiation to allopatry and nonadaptive divergence. Phylogenetic approaches to locating the most appropriate speciation models have been constrained by the low levels of molecular divergence between recently diverged species, which are typical of recent, rapid radiations. In this issue of Molecular Ecology, Rymer et al. (2010) used coalescence analyses of sequence data and genome scans of Amplified Fragment Length Polymorphism (AFLP) loci to demonstrate that in a species complex in the irid genus Gladiolus, a member of the hyper diverse Cape flora of southern Africa, speciation is a gradual process. Older divergences are genetically more differentiated, and show a greater difference in flowering time and floral morphology, than taxa that diverged more recently. There is no evidence of any abrupt events. Gene flow is limited by shifts in flowering time and floral morphology; thus, by pre-zygotic rather than by post-zygotic mechanisms, these evolved together with the occupation of somewhat different habitats. This research gives the first critical insight into how the remarkable diversity in a diversity hotspot could have arisen. More importantly, it demonstrates that the speciation process in recent, rapid radiations is tractable and can be investigated with suitable genetic tools.     

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.