Genome sequences of Tropheus moorii and Petrochromis trewavasae, two eco-morphologically divergent cichlid fishes endemic to Lake Tanganyika.

With more than 1000 species, East African cichlid fishes represent the fastest and most species-rich vertebrate radiation known, providing an ideal model to tackle molecular mechanisms underlying recurrent adaptive diversification. We add high-quality genome reconstructions for two phylogenetic key species of a lineage that diverged about ~ 3-9 million years ago (mya), representing the earliest split of the so-called modern haplochromines that seeded additional radiations such as those in Lake Malawi and Victoria. Along with the annotated genomes we analysed discriminating genomic features of the study species, each representing an extreme trophic morphology, one being an algae browser and the other an algae grazer. The genomes of Tropheus moorii (TM) and Petrochromis trewavasae (PT) comprise 911 and 918 Mbp with 40,300 and 39,600 predicted genes, respectively. Our DNA sequence data are based on 5 and 6 individuals of TM and PT, and the transcriptomic sequences of one individual per species and sex, respectively. Concerning variation, on average we observed 1 variant per 220 bp (interspecific), and 1 variant per 2540 bp (PT vs PT)/1561 bp (TM vs TM) (intraspecific). GO enrichment analysis of gene regions affected by variants revealed several candidates which may influence phenotype modifications related to facial and jaw morphology, such as genes belonging to the Hedgehog pathway (SHH, SMO, WNT9A) and the BMP and GLI families.

Male courtship preferences demonstrate discrimination against allopatric colour morphs in a cichlid fish.

Whether premating isolation is achieved by male-specific, female-specific or sex-independent assortative preferences often depends on the underlying evolutionary processes. Here we test mate preferences of males presented with females of different allopatric colour variants of the cichlid fish Tropheus sp., a Lake Tanganyika endemic with rich geographical colour pattern variation, in which the strength of sexual isolation varies between populations. We conducted two-way mate choice experiments to compare behaviour of males of a red-bodied morph (population Moliro) towards females from their own population with behaviour towards females from four allopatric populations at different stages of phylogenetic and phenotypic divergence. Males courted same-population females significantly more intensely than females of other populations, and reduced their heteromorphic courtship efforts both with increasing genetic and increasing phenotypic distinctness of the females. In particular, females of a closely related red-bodied population received significantly more courtship than either genetically distinct, similarly coloured females ('Kirschfleck' morph) or genetically related, differently coloured females ('yellow-blotch' morph), both of which were courted similarly. Genetically and phenotypically distinct females (Tropheus polli) were not courted at all. Consistent with previous female-choice experiments, female courtship activity also decreased with increasing genetic distance from the males' population. Given successful experimental and natural introgression between colour morphs and the pervasive allopatry of related variants, we consider it unlikely that assortative preferences of both sexes were driven by direct selection during periods of secondary contact or, in turn, drove colour pattern differentiation in allopatry. Rather, we suggest that sexual isolation evolved as by-product of allopatric divergence.

Ancient origin and recent divergence of a haplochromine cichlid lineage from isolated water bodies in the East African Rift system.

Phylogenetic analysis identified haplochromine cichlids from isolated water bodies in the eastern branch of the East African Rift system as an ancient lineage separated from their western sister group in the course of the South Kenyan-North Tanzanian rift system formation. Within this lineage, the close phylogenetic relatedness among taxa indicates a recent common ancestry and historical connections between now separated water bodies. In connection with a total lack of local genetic diversity attributable to population bottlenecks, the data suggest cycles of extinction and colonization in the unstable habitat provided by the small lakes and rivers in this geologically highly active area.

Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish.

We used nuclear and mitochondrial DNA (mtDNA) sequences from specimens collected throughout Lake Tanganyika to clarify the evolutionary relationship between Lamprologus callipterus and Neolamprologus fasciatus. The nuclear data support the reciprocal monophyly of these two shell-breeding lamprologine cichlids. However, mtDNA sequences show that (i) L. callipterus includes two divergent and geographically disjunct (North-South) mtDNA lineages; and that (ii) N. fasciatus individuals cluster in a lineage sister group to the northern lineage of L. callipterus. The two mtDNA lineages of L. callipterus diverged c. 684 kya to 1.2 Ma, coinciding with a major water level low stand in Lake Tanganyika, which divided the lake into isolated sub-lakes. This suggests that the two mtDNA lineages originated as the result of the separation of L. callipterus populations in different sub-basins. The incongruent phylogenetic position of N. fasciatus can best be explained by an ancient unidirectional introgression from L. callipterus into N. fasciatus. Remarkably, our data indicate that this event resulted in the complete mtDNA replacement in N. fasciatus. Our data suggest that hybridization occurred soon after the divergence of the two L. callipterus mtDNA lineages, probably still during the water level low stand, and that subsequently the invading mtDNA lineage spread throughout the lake.

Mating system variability in a mouthbrooding cichlid fish from a tropical lake.

Intraspecific variability in mating behaviour and disparities between social and reproductive behaviour add complexity to the description of animal mating systems. A previously published field study on a population of the maternally mouthbrooding cichlid fish Ctenochromis horei in the north of Lake Tanganyika suggested mate monopolization by the most dominant male. In the present study, genetic reconstructions of paternity in a population in the south of the lake provided no evidence for male mate monopolization, as none of the inferred sires had offspring in more than one brood. The ability to reconstruct sire genotypes from offspring alleles was confirmed by computer simulations. Multiple paternity occurred in several broods and was significantly more frequent in the sample taken in the rainy season than in the dry season sample (100% of broods vs. 14%, respectively; P = 0.005). The data suggest geographical and temporal variation in the mating behaviour of C. horei despite its continuous year-round reproduction, invariable brood care behaviour and habitat-specific distribution in the relatively constant and confined environment of a tropical lake. Moreover, our data show that inferences on the distribution of male reproductive success, if based on each geographical or temporal data set alone, would fail to describe the potential for sexual selection in this species.

A single mitochondrial haplotype and nuclear genetic differentiation in sympatric colour morphs of a riverine cichlid fish.

Some of the diversity of lacustrine cichlid fishes has been ascribed to sympatric divergence, whereas diversification in rivers is generally driven by vicariance and geographic isolation. In the riverine Pseudocrenilabrus philander species complex, several morphologically highly distinct populations are restricted to particular river systems, sinkholes and springs in southern Africa. One of these populations consists of a prevalent yellow morph in sympatry with a less frequent blue morph, and no individuals bear intermediate phenotypes. Genetic variation in microsatellites and AFLP markers was very low in both morphs and one single mtDNA haplotype was fixed in all samples, indicating a very young evolutionary age and small effective population size. Nevertheless, the nuclear markers detected low but significant differentiation between the two morphs. The data suggest recent and perhaps sympatric divergence in the riverine habitat.