Molecular genetics of explosive speciation in cichlid fishes

The proposed research focuses on the process of adaptive radiation, an evolutionary phenomenon, during which a multitude of new species is generated in a short period of time. The East African lakes with their flocks of cichlid fishes have been established as model system to study major diversification events. Lake Tanganyika, the second oldest lake in the world, is particularly interesting, since the process of adaptive radiation is in a highly advanced stage. The community of cichlid fishes has reached a level of diversity that is unsurpassed in any freshwater system. In contrast to the cichlids of Lakes Malawi and Victoria, species from Lake Tanganyika are clearly demarkated in terms of ecology, morphology and genetic divergence. Incomplete lineage sorting above the species level does not occur in Lake Tanganyika cichlids. The species flock is of polyphyletic origin and five seeding lineages underwent radiation. Taken together, these circumstances offer a unique opportunity to compare independent sub-radiations of cichlid fishes that were triggered by exactly the same external modulators in form of geological events and fluctuations of the lake level, and to study the influence of external and biological factors on the pathways of diversification. Our research builds on the results of our previous grant and intends to complete the molecular phylogeny of the whole species flock by adding data of deepwater species, and to continue our population genetic and ecological studies to better understand incipient speciation on the population level. Specifically, we tackle four goals: (1) To elaborate a comprehensive phylogeny of the Lamprologini, the Bathybatini and the Trematocarini; (2) to compare temporary and ecological patterns of diversification in the Lamprologini, the Trematocarini and the Bathybatini to those observed in the H-lineage and the Eretmodini; (3) to study patterns of ecological and genetic divergence on the population level by comparing the genetic structure of a set of sympatric substrate-breeding species over a shore line of about 30 km and to relate these results to the findings on mouthbrooding species from our previous grant; and (4) to establish an age calibration system based on otoliths for three model cichlid species to understand the age structure of cichlid communities. The project includes a cooperation with the University of Lusaka and the Fisheries Department of the Republic of Zambia.

The history of life on earth shows a pattern: recurrent periods if intensive innovation, termed radiation, are interleaved by periods of relative stasis. Our project intended to address specific pathways and mechanisms driving the evolution of complex species communities within a short period of time. The flocks of East African cichlid fishes in Lakes Victoria, Malawi and Tanganyika, each counting hundreds of endemic species, represent excellent model systems to study ongoing explosive speciation and adaptive radiation. We concentrated on the species flock of Lake Tanganyika to trace the pathways of diversification in this highly complex array of cichlid fishes. Unlike in the other lakes, the cichlids of Lake Tanganyika are of polyphyletic origin, so that several ancestors seeded the radiation and independently underwent diversification into more or less species-rich lineages. We first continued our work from previous grants to elucidate the phylogenetic relationships of the entire species flock, used the phylogenetic hypotheses to trace pathways of progressive specialization to a wide variety of ecological niches, and then addressed specific ecological and biological parameters of the studied species which are necessary to be known in order to adequately model the diversification process. Our work resulted in 10 publications in high- ranked international journals, 3 book contributions and one popular scientific publication. We presented a phylogeny of the entire Lake Tanganyika species flock and showed that the radiation of the "haplochromine cichlids", which colonized many other African water bodies and seeded the radiation in Lakes Victoria and Malawi, had its roots within the Lake Tanganyika radiation, constraining its origin to the early Lake Tanganyika basin at a time when the lake ecosystem was not yet isolated from other water bodies by the formation of the East African rift. Moreover, we presented the first "hard evidence" that - under particular environmental conditions - hybridization among highly distinct animal species can lead to the formation of new species, a phenomenon that was only recognized for plant species so far. In several publications we showed by comparative analysis of genetic divergences that lake level fluctuations induced by climate changes are important modulators of the speciation process. Such major habitat changes induce diversification in independent lineages, and so act as temporary synchronizers of the radiation process among lineages. Also, we describe several cases in which even complex trophic adaptations and breeding behaviors evolved more than once within a single lake, highlighting an interesting characteristic of directional selection which is prone to take the same route of adaptation when independently starting from the same "starting point" in geographically isolated populations. Concerning biological parameters influencing the pace and route of the radiation process we were the first to tackle the age structure in cichlid populations. Thereby we showed that cichlids can grow as old as 10 years and that the generation time amounts to 4 years