Phylogenomics uncovers early hybridization and adaptive loci shaping the radiation of Lake Tanganyika cichlid fishes

Iker Irisarri,Christian Sturmbauer,Julián Torres-Dowdall,Frederico Henning,Paolo Franchini,Emily Moriarty Lemmon,Pooja Singh,Axel Meyer,Gerhard G Thallinger,Stephan Koblmüller,Alan R Lemmon,Christoph Fischer

doi:10.1038/s41467-018-05479-9

Abstract

Lake Tanganyika is the oldest and phenotypically most diverse of the three East African cichlid fish adaptive radiations. It is also the cradle for the younger parallel haplochromine cichlid radiations in Lakes Malawi and Victoria. Despite its evolutionary significance, the relationships among the main Lake Tanganyika lineages remained unresolved, as did the general timescale of cichlid evolution. Here, we disentangle the deep phylogenetic structure of the Lake Tanganyika radiation using anchored phylogenomics and uncover hybridization at its base, as well as early in the haplochromine radiation. This suggests that hybridization might have facilitated these speciation bursts. Time-calibrated trees support that the radiation of Tanganyika cichlids coincided with lake formation and that Gondwanan vicariance concurred with the earliest splits in the cichlid family tree. Genes linked to key innovations show signals of introgression or positive selection following colonization of lake habitats and species’ dietary adaptations are revealed as major drivers of colour vision evolution. These findings shed light onto the processes shaping the evolution of adaptive radiations.

Highlights

Lake Tanganyika is the oldest and phenotypically most diverse of the three East African cichlid fish adaptive radiations
The rapid diversification of East African cichlids has been attributed to key innovations including (i) functional decoupling of oral and pharyngeal jaws facilitating exploitation of diverse trophic sources[20], (ii) vision adaptation to different water turbidity[21], and (iii) body coloration associated with sexual selection and reproductive isolation[22]
The divergence times estimated here are in accordance with two major geological events in cichlid history: the radiation of the Lake Tanganyika species flock coincides with the lake formation, and the deepest splits in the cichlid tree agree with Gondwanan vicariance

Summary

Introduction

Lake Tanganyika is the oldest and phenotypically most diverse of the three East African cichlid fish adaptive radiations. Disentangling the geographical setting, ecology, genetic causes, commonalities and peculiarities in different adaptive radiations has proven difficult[6,7] Sudden abiotic changes such as new volcanic islands or lakes can provide empty niches that facilitate diversification. A robust phylogenetic hypothesis for cichlids will resolve existing controversies but it will allow to understand the origin and evolution of key innovations, life history changes, and further clarify the patterns of convergence and parallel evolution that characterize cichlid radiations. The rapid diversification of East African cichlids has been attributed to key innovations including (i) functional decoupling of oral and pharyngeal jaws facilitating exploitation of diverse trophic sources[20], (ii) vision adaptation to different water turbidity[21], and (iii) body coloration associated with sexual selection and reproductive isolation[22]. The lack of studies simultaneously modelling different ecological and life-history factors hampers the identification of hierarchical relationships among them, as well as the identification of lineage-specific shifts[6]

Methods

Results

Conclusion