Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration

Abstract

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...

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“…Disentangling the relative contributions of variation shared since ancestry and shared via gene flow is necessary for estimating the time since speciation and for assessing speciation models. Recently, with the use of very large numbers of amplified fragment-length polymorphisms (9,10), it has become possible to estimate phylogenetic trees. However, it is difficult to model the substitution process for these markers and therefore it is difficult to use amplified fragment-length polymorphisms to estimate the time since speciation events.…”

“…The fact of shared variation means that neither allelic nor haplotypic data from individual loci (or from a small number of loci) can provide phylogenetic resolution (5)(6)(7), and in recent years investigators have had to turn to using very large numbers of amplified fragment-length polymorphism markers to estimate phylogenies (9,10).…”

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