Taxon boundaries in the early stages of divergence

The early stages of diversification, during which differentiation between populations depends mainly on geographic conditions, the local environment and the ecology and behavior of the organism, afford opportunities to study how the interplay of these external and internal factors act on the evolution of genetic structure and reproductive barriers. The cichlid fishes of the Great Lakes in East Africa are renowned model systems for studies of phenotypic and genetic diversification. In Lake Tanganyika, the endemic genus Tropheus represents the most impressive example for allo- and parapatric variation in body color pattern, with over 100 recognized morphs. The morphs are separated by different levels of reproductive isolation and genetic and phenotypic differentiation, and are considered to represent different stages on the way to speciation. Yet, diversification and speciation processes between Tropheus taxa rely on pre-mating isolation and are, at least in theory, still reversible, especially when allopatric diversification is interrupted by periods of secondary contact due to lake level fluctuations. Tropheus therefore represent an excellent system to address the evolutionary dynamics among closely related, yet phenotypically and genetically divergent populations. Furthermore, the large number of different color morphs provides natural replicates and thus allows for broader inferences on interactions between differentiated morphs. The observation of single paternity of clutches and morph-specific differences in assortative mate preferences as well as the general absence of sexual dimorphism raised doubts that sexual selection played an equally important role in Tropheus as is hypothesized for the haplochromine radiations of Lakes Malawi and Victoria. Furthermore, the analyses of phylogeography and population structure of Tropheus indicated philopatry and genetic differentiation on the one hand and introgression associated with lake level fluctuations on the other hand, which suggests that diversification processes may be affected by cycles of allopatric differentiation and secondary contact. Building on previous work, the present proposal seeks to investigate the balance between reproductive isolation and introgression between parapatric color morphs of Tropheus by means of an integrative approach combining population genetic analysis and behavioral (i.e., mate choice) experiments. Specifically, the proposed experiments examine (1) whether patterns of genetic introgression between color morphs can be related to mating preferences observed in lab experiments, (2) whether major habitat disturbances (e.g. drops in the lake level) have the potential to induce hybridization between well-differentiated morphs, and (3) whether mate preferences observed in lab experiments are robust against experimental modifications - in particular whether male territories influence female mating decisions, given that field studies suggest resource-dependent mating success in Tropheus males. Experiments will test whether assortative female mate preferences can be reversed by differences between male resources benefiting the heteromorphic male. Molecular techniques (AFLP and microsatellite genotyping, SNP and HapSTR analysis, DNA sequencing) will be combined with modern analysis methods (based on Bayesian inference, coalescence theory) and behavioral data to disentangle environmental, behavioral, and stochastic (drift) influences on genetic structure and diversification.

The project looked at the evolution of closely related, geographically separated populations. The study system is a fish species, Tropheus moorii, which is one of the many cichlid fishes occurring only in Lake Tanganyika, Africa. The most outstanding feature of Tropheus is its rich geographic variation in body colouration almost every population can be distinguished by its own specific colour pattern. Tropheus inhabit the shallow rocky zone along the lakes shoreline, and populations are separated from each other by habitat barriers such as sandy stretches formed by river estuaries. These barriers are not permanent across geological timescales. Lake level fluctuations have repeatedly caused the shoreline to shrink and expand, and the fish communities had to move along with their changing habitat. Oftentimes, this forced formerly separated populations into so-called secondary contact . Work in this project investigated the influences of secondary contact between populations with different body colour (colour morphs) on the evolution of the stunning colour pattern diversity within this species. Experiments on mate choice and male-male competition between colour morphs showed that sexual and competitive interactions between individuals were influenced by body colour. Red males dominate over males of other colours, and mate preferences for own-type partners are strong in the red morph, but weak in another and absent in a third morph. Our studies predict that secondary contact between the investigated morphs would lead to interbreeding and admixture of morphs, and demonstrate that interactions between male-male competition and mate preferences shape the patterns of mate choice. What are the consequences of hybridization between morphs? Using population genetic tools, we found that a particular yellow-coloured morph originated from ancient hybridization between red and bluish populations. Moreover, crossing red and bluish Tropheus in the lab produced yellow-coloured offspring as well. Currently, the red and bluish populations are located north and south, respectively, from their hybrid product. The estuary of a large river forms a major habitat barrier in this area. Our data suggest that a drought and the drop of the lake level in the Late Pleistocene eliminated this barrier and led to contact between the red and bluish Tropheus. The novel yellow morph emerged by interbreeding, while the parental morphs continued to exist pure further away from the contact zone. With a subsequent rise in lake level, barriers between the old and the new morphs were reinforced and have been keeping the now three different morphs in geographic isolation. Analyses of hybrid populations in another contact zone suggested an analogous scenario, and provide a second empirical example of how spatially restricted hybridization between colour morphs promotes the evolution of colour pattern diversity in this system.