Genetic architecture of a key reproductive isolation trait differs between sympatric and non-sympatric sister species of Lake Victoria cichlids.

One hallmark of the East African cichlid radiations is the rapid evolution of reproductive isolation that is robust to full sympatry of many closely related species. Theory predicts that species persistence and speciation in sympatry with gene flow are facilitated if loci of large effect or physical linkage (or pleiotropy) underlie traits involved in reproductive isolation. Here, we investigate the genetic architecture of a key trait involved in behavioural isolation, male nuptial coloration, by crossing two sister species pairs of Lake Victoria cichlids of the genus Pundamilia and mapping nuptial coloration in the F2 hybrids. One is a young sympatric species pair, representative of an axis of colour motif differentiation, red-dorsum versus blue, that is highly recurrent in closely related sympatric species. The other is a species pair representative of colour motifs, red-chest versus blue, that are common in allopatric but uncommon in sympatric closely related species. We find significant quantitative trait loci (QTLs) with moderate to large effects (some overlapping) for red and yellow in the sympatric red-dorsum × blue cross, whereas we find no significant QTLs in the non-sympatric red-chest × blue cross. These findings are consistent with theory predicting that large effect loci or linkage/pleiotropy underlying mating trait differentiation could facilitate speciation and species persistence with gene flow in sympatry.

A Dense Linkage Map of Lake Victoria Cichlids Improved the Pundamilia Genome Assembly and Revealed a Major QTL for Sex-Determination.

Genetic linkage maps are essential for comparative genomics, high quality genome sequence assembly and fine scale quantitative trait locus (QTL) mapping. In the present study we identified and genotyped markers via restriction-site associated DNA (RAD) sequencing and constructed a genetic linkage map based on 1,597 SNP markers of an interspecific F2 cross of two closely related Lake Victoria cichlids (Pundamilia pundamilia and P sp. 'red head'). The SNP markers were distributed on 22 linkage groups and the total map size was 1,594 cM with an average marker distance of 1.01 cM. This high-resolution genetic linkage map was used to anchor the scaffolds of the Pundamilia genome and estimate recombination rates along the genome. Via QTL mapping we identified a major QTL for sex in a ∼1.9 Mb region on Pun-LG10, which is homologous to Oreochromis niloticus LG 23 (Ore-LG23) and includes a well-known vertebrate sex-determination gene (amh).

Sequential female assessment drives complex sexual selection on bower shape in a cichlid fish.

In many animals, sexual selection on male traits results from female mate choice decisions made during a sequence of courtship behaviors. We use a bower-building cichlid fish, Nyassachromis cf. microcephalus, to show how applying standard selection analysis to data on sequential female assessment provides new insights into sexual selection by mate choice. We first show that the cumulative selection differentials confirm previous results suggesting female choice favors males holding large volcano-shaped sand bowers. The sequential assessment analysis reveals these cumulative differentials are the result of selection acting on different bower dimensions during the courtship sequence; females choose to follow males courting from tall bowers, but choose to engage in premating circling with males holding bowers with large diameter platforms. The approach we present extends standard selection analysis by partitioning the variances of increasingly accurate estimates of male reproductive fitness and is applicable to systems in which sequential female assessment drives sexual selection on male traits.

Establishment and expansion of Lake Malawi rock fish populations after a dramatic Late Pleistocene lake level rise.

Major environmental events that fragment populations among multiple island habitats have potential to drive large-scale episodes of speciation and adaptive radiation. A recent palaeolimnological study of sediment cores indicated that Lake Malawi underwent major climate-driven desiccation events 75,000-135,000 years ago that lowered the water level to at least 580 m below the present state and severely reduced surface area. After this period, lake levels rose and stabilized, creating multiple discontinuous littoral rocky habitats. Here, we present evidence supporting the hypothesis that establishment and expansion of isolated philopatric rock cichlid populations occurred after this rise and stabilization of lake level. We studied the Pseudotropheus (Maylandia) species complex, a group with both allopatric and sympatric populations that differ in male nuptial colour traits and tend to mate assortatively. Using coalescent analyses based on mitochondrial DNA, we found evidence that populations throughout the lake started to expand and accumulate genetic diversity after the lake level rise. Moreover, most haplotypes were geographically restricted, and the greatest genetic similarities were typically among sympatric or neighbouring populations. This is indicative of limited dispersal and establishment of assortative mating among populations following the lake level rise. Together, this evidence is compatible with a single large-scale environmental event being central to evolution of spatial patterns of genetic and species diversity in P. (Maylandia) and perhaps other Lake Malawi rock cichlids. Equivalent climate-driven pulses of habitat formation and fragmentation may similarly have contributed to observed rapid and punctuated cladogenesis in other adaptive radiations.

Heritability and heterochrony of polychromatism in a Lake Victoria Cichlid fish: Stepping stones for speciation?

In many haplochromine cichlid fish, male nuptial coloration is subject to female mate choice and plays a central role in the evolution of reproductive isolation between incipient species. Intraspecific variation in male coloration may serve as a target for diversifying sexual selection and provide a starting point for species divergence. Here, we investigated a polychromatism in Neochromis omnicaeruleus, a haplochromine from Lake Victoria, East-Africa. In this species, male coloration ranges from skyblue to yellow-red and females are grey-blue to yellow. We found that both genetic and environmental factors influence the expression of these colours during individual development. In a natural population, we found that male colour was associated with size and sexual maturity: yellow males were smaller than blue males and tended to be sexually immature. In females, size and maturity did not differ between colour types. Laboratory crosses revealed that there is a heritable component to the observed colour variation: yellow parents produced more yellow offspring than blue parents. Together with repeated aquarium observations of yellow individuals that gradually become blue, these data suggest that yellow males change to blue as they approach sexual maturity, and that the occurrence and timing of this transition is influenced by both environmental and genetic effects. The significance of this mechanism of colour expression as a possible target for divergent selection remains to be evaluated.

Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation.

Female mate choice has often been proposed to play an important role in cases of rapid speciation, in particular in the explosively evolved haplochromine cichlid species flocks of the Great Lakes of East Africa. Little, if anything, is known in cichlid radiations about the heritability of female mating preferences. Entirely sympatric distribution, large ecological overlap and conspicuous differences in male nuptial coloration, and female preferences for these, make the sister species Pundamilia pundamilia and P. nyererei from Lake Victoria an ideally suited species pair to test assumptions on the genetics of mating preferences made in models of sympatric speciation. Female mate choice is necessary and sufficient to maintain reproductive isolation between these species, and it is perhaps not unlikely therefore, that female mate choice has been important during speciation. A prerequisite for this, which had remained untested in African cichlid fish, is that variation in female mating preferences is heritable. We investigated mating preferences of females of these sister species and their hybrids to test this assumption of most sympatric speciation models, and to further test the assumption of some models of sympatric speciation by sexual selection that female preference is a single-gene trait. We find that the differences in female mating preferences between the sister species are heritable, possibly with quite high heritabilities, and that few but probably more than one genetic loci contribute to this behavioural speciation trait with no apparent dominance. We discuss these results in the light of speciation models and the debate about the explosive radiation of cichlid fishes in Lake Victoria.