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 yellowin 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

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

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth-brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth-brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth-brooding cichlids is discussed

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

Recent sympatric speciation involving habitat-associated nuptial colour polymorphism in a crater lake cichlid

Even though the idea that modes of speciation other than allopatric speciation are possible in nature is now widespread, compelling examples of ecological speciation in sympatry remain rare. We studied an undescribed radiation of haplochromine cichlids in a young crater lake in western Uganda, and in the small river that is nearby but has currently no known surface connection to the lake. We describe two different modes of speciation that occurred in this cichlid lineage within the past 1,500–10,000 years. Not constrained by gene flow, allopatric divergence between river and lake cichlids affects many different morphological traits as well as nuptial colouration - muted in the river, but intensified and polymorphic in lake cichlids - and neutral genetic differentiation. More surprisingly, we demonstrate a case for sympatric speciation within the small lake that is associated with dramatic differences in male breeding colouration (yellow with bright red-chest versus bright blue) and subtle differences in microhabitat, feeding regime and morphology. Reproductive isolation by assortative mating is suggested by significant differentiation between yellow and blue males in neutral markers of gene flow despite complete sympatry. We hypothesize speciation is mediated by divergent selection on sexual signalling between microhabitats

Microtomographic investigation of a large corpus of cichlids.

A large collection of cichlids (N = 133) from Lake Victoria in Africa, with total lengths ranging from 6 to 18 cm was nondestructively imaged using micro-computed tomography. We present a method to efficiently obtain three-dimensional tomographic datasets of the oral and pharyngeal jaws and the whole skull of these fishes to accurately describe their morphology. The tomographic data we acquired (9.8 TB of projection images) yielded 1.5 TB of three-dimensional image stacks used for extracting the relevant features of interest. Herein we present our method and outlooks on analyzing the acquired data; a morphological description of the oral and pharyngeal jaws, a three-dimensional geometric morphometrics analysis of landmarked skull features, and a robust method to automatically extract otoliths from the tomographic data

Visualization of automatic otolith extraction.

The top row shows the found location of the otolith center in each of the three anatomical directions. The bottom row shows a maximum intensity projection of each of the three anatomical directions of the extracted otolith region.</p

Three-dimensional view of extracted otoliths of specimen 104016.

The specimen was scanned with an isotropic voxel size of 13 μm. The extracted otolith has a size of approximately 250 x 350 x 150 pixels. The axes labels correspond to mm. A dynamic view of the visualization is available in the Supporting information.</p