The genomic causes and effects of divergent ecological selection during speciation are still poorly understood. Here, we report the discovery and detailed characterization of early-stage adaptive divergence of two cichlid fish ecomorphs in a small (700m diameter) isolated crater lake in Tanzania. The ecomorphs differ in depth preference, male breeding color, body shape, diet and trophic morphology. With whole genome sequences of 146 fish, we identify 98 clearly demarcated genomic 'islands' of high differentiation and demonstrate association of genotypes across these islands to divergent mate preferences. The islands contain candidate adaptive genes enriched for functions in sensory perception (including rhodopsin and other twilight vision associated genes), hormone signaling and morphogenesis. Our study suggests mechanisms and genomic regions that may play a role in the closely related mega-radiation of Lake Malawi. * Publisher's Disclaimer: This manuscript has been accepted for publication in Science. This version has not undergone final editing.Please refer to the complete version of record at http://www.sciencemag.org/. The manuscript may not be reproduced or used in any manner that does not fall within the fair use provisions of the
Timing divergence events allow us to infer the conditions under which biodiversity has evolved and gain important insights into the mechanisms driving evolution. Cichlid fishes are a model system for studying speciation and adaptive radiation, yet, we have lacked reliable timescales for their evolution. Phylogenetic reconstructions are consistent with cichlid origins prior to Gondwanan landmass fragmentation 121-165 MYA, considerably earlier than the first known fossil cichlids (Eocene). We examined the timing of cichlid evolution using a relaxed molecular clock calibrated with geological estimates for the ages of 1) Gondwanan fragmentation and 2) cichlid fossils. Timescales of cichlid evolution derived from fossil-dated phylogenies of other bony fishes most closely matched those suggested by Gondwanan breakup calibrations, suggesting the Eocene origins and marine dispersal implied by the cichlid fossil record may be due to its incompleteness. Using Gondwanan calibrations, we found accumulation of genetic diversity within the radiating lineages of the African Lakes Malawi, Victoria and Barombi Mbo, and Palaeolake Makgadikgadi began around or after the time of lake basin formation. These calibrations also suggest Lake Tanganyika was colonized independently by the major radiating cichlid tribes that then began to accumulate genetic diversity thereafter. These results contrast with the widely accepted theory that diversification into major lineages took place within the Tanganyika basin. Together, this evidence suggests that ancient lake habitats have played a key role in generating and maintaining diversity within radiating lineages and also that lakes may have captured preexisting cichlid diversity from multiple sources from which adaptive radiations have evolved.
The spatial distribution of neutral genetic diversity is mainly influenced by barriers to dispersal. The nature of such barriers varies according to the dispersal means and capabilities of the organisms concerned. Although these barriers are often obvious on land, in the ocean they can be more difficult to identify. Determining the relative influence of physical and biotic factors on genetic connectivity remains a major challenge for marine ecologists. Here, we compare gene flow patterns of 7 littoral fish species from 6 families with a range of early-life-history traits sampled at the same geographic locations across common environmental discontinuities in the form of oceanic fronts in the Western Mediterranean. We show that these fronts represent major barriers to gene flow and have a strong influence on the population genetic structure of some fish species. We also found no significant relation between the early-life-history traits most commonly investigated (egg type, pelagic larval duration, and inshore-offshore spawning) and gene flow patterns, suggesting that other life-history factors should deserve attention. The fronts analyzed and the underlying physical mechanisms are not site-specific but common among the oceans, suggesting the generality of our findings.gene flow ͉ microsatellite ͉ ocean circulation ͉ pelagic stages
Repeated evolution of the same phenotypic difference during independent episodes of speciation is strong evidence for selection during speciation. More than 1,000 species of cichlids, >10% of the world's freshwater fish species, have arisen within the past million years in Lakes Malawi and Victoria in eastern Africa. Many pairs of closely related sympatric species differ in their nuptial coloration in very similar ways. Nuptial coloration is important in their mate choice, and speciation by sexual selection on genetically or ecologically constrained variation in nuptial coloration had been proposed, which would repeatedly produce similar nuptial types in different populations, a prediction that was difficult to test in the absence of population-level phylogenies. We measured genetic similarity between individuals within and between populations, species, and lake regions by typing 59 individuals at >2,000 polymorphic genetic loci. From these data, we reconstructed, to our knowledge, the first larger species level phylogeny for the most diverse group of Lake Malawi cichlids. We used the genetic and phylogenetic data to test the divergent selection scenario against colonization, character displacement, and hybridization scenarios that could also explain diverse communities. Diversity has arisen by replicated radiations into the same color types, resulting in phenotypically very different, yet closely related, species within and phenotypically highly similar yet unrelated sets of species between regions, which is consistent with divergent selection during speciation and is inconsistent with colonization and character displacement models. R epeated differentiation into the same pairs of ecological or mating phenotypes during independent episodes of speciation is strong evidence for speciation by selection (1-3). Because species continue to diverge in other traits after speciation, such pairs are most readily detected where many species have recently diverged from few ancestors, as in geologically young adaptive radiations (4). The haplochromine cichlids in Lakes Victoria and Malawi in eastern Africa (5) form the largest recent adaptive radiations of vertebrates and account for Ͼ10% of the world's freshwater fish species (6-8). Parallel origins of similar morphologies in different lakes has been documented (9), but closely related species within each lake generally have similar morphologies (10), but differ in nuptial color patterns, often in similar ways (11-13). Nuptial coloration is important in their mate choice (13,14) and speciation by sexual selection on genetically or ecologically constrained variation in nuptial coloration had been proposed to explain its rapid evolution (15, 16). Other candidate explanations include genetic drift in small populations and reproductive character displacement in secondary sympatry.Even in the stenotopic rock-dwelling Mbuna group, populations rarely show the genetic imprints of bottlenecks (6,17), and the number of migrants between populations is typically too large for divergen...
The endemic cichlid fishes of Lakes Malawi, Tanganyika and Victoria are textbook examples of explosive speciation and adaptive radiation, and their study promises to yield important insights into these processes. Accurate estimates of species richness of lineages in these lakes, and elsewhere, will be a necessary prerequisite for a thorough comparative analysis of the intrinsic and extrinsic factors influencing rates of diversification. This review presents recent findings on the discoveries of new species and species flocks and critically appraises the relevant evidence on species richness from recent studies of polymorphism and assortative mating, generally using behavioural and molecular methods. Within the haplochromines, the most species-rich lineage, there are few reported cases of postzygotic isolation, and these are generally among allopatric taxa that are likely to have diverged a relatively long time in the past. However, many taxa, including many which occur sympatrically and do not interbreed in nature, produce viable, fertile hybrids. Prezygotic barriers are more important, and persist in laboratory conditions in which environmental factors have been controlled, indicating the primary importance of direct mate preferences. Studies to date indicate that estimates of alpha (within-site) diversity appear to be robust. Although within-species colour polymorphisms are common, these have been taken into account in previous estimates of species richness. However, overall estimates of species richness in Lakes Malawi and Victoria are heavily dependent on the assignation of species status to allopatric populations differing in male colour. Appropriate methods for testing the specific status of allopatric cichlid taxa are reviewed and preliminary results presented.
Mechanisms behind the explosive radiation of over 500 cichlid ¢sh species from a single founding population in Lake Malawi during the last 700 000 years are poorly understood. Recent studies have suggested that the degree of population subdivision among the habitat patches within the lake may be responsible, but the evidence has been circumstantial: lack of a dispersal stage in haplochromine cichlids; genetic and colour variation among populations separated by large-scale geographical barriers; and £uctuating lake levels. One reason for the rapidity of speciation in these ¢shes may be that population subdivision is on a much ¢ner scale than previously thought. Here we quantify the level of population subdivision and estimate migration at a scale of 700^1400 m, in order to investigate whether cichlid populations are su¤ciently isolated from each other for allopatric divergence and perhaps speciation to take place. Using six microsatellite loci, we demonstrate the existence of highly signi¢cant genetic di¡erentiation between subpopulations on adjacent headlands in each of four rock-dwelling haplochromine cichlid species. Our results suggest that these ¢sh populations are divided into thousands of subunits among which genetic divergence is currently occurring, and that this may provide unprecedented opportunities for allopatric speciation.
The haplochromine cichlid fish of the East African Great Lakes represent some of the fastest and most species-rich adaptive radiations known, but rivers in most of Africa accommodate only a few morphologically similar species of haplochromine cichlid fish. This has been explained by the wealth of ecological opportunity in large lakes compared with rivers. It is therefore surprising that the rivers of southern Africa harbour many, ecologically diverse haplochromines. Here we present genetic, morphological and biogeographical evidence suggesting that these riverine cichlids are products of a recent adaptive radiation in a large lake that dried up in the Holocene. Haplochromine species richness peaks steeply in an area for which geological data reveal the historical existence of Lake palaeo-Makgadikgadi. The centre of this extinct lake is now a saltpan north of the Kalahari Desert, but it once hosted a rapidly evolving fish species radiation, comparable in morphological diversity to that in the extant African Great Lakes. Importantly, this lake seeded all major river systems of southern Africa with ecologically diverse cichlids. This discovery reveals how local evolutionary processes operating during a short window of ecological opportunity can have a major and lasting effect on biodiversity on a continental scale.
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