The genomic timeline of cichlid fish diversification across continents

Abstract

Cichlid fishes are celebrated for their vast taxonomic, phenotypic, and ecological diversity; however, a central aspect of their evolution - the timeline of their diversification - remains contentious. Here, we generate draft genome assemblies of 14 species representing the global cichlid diversity and integrate these into a new phylogenomic hypothesis of cichlid and teleost evolution that we time-calibrate with 58 re-evaluated fossil constraints and a new Bayesian model accounting for fossil-assignment uncertainty. Our results support cichlid diversification long after the breakup of the supercontinent Gondwana and lay the foundation for precise temporal reconstructions of the exceptional continental cichlid adaptive radiations.

Fig. 1. Global distribution of cichlid fishes and diversification scenarios.

a Present-day distribution of cichlid fishes in the Americas (subfamily Cichlinae; blue), Africa, and the Levant (Pseudocrenilabrinae; cyan), Madagascar (Ptychochrominae; green), and the Indian subcontinent (Etroplinae; orange). The drawings illustrate the 14 cichlid species used for whole-genome sequencing. Their approximate geographic origins are indicated. b Three hypotheses for the phylogeographic history of cichlid fishes. According to the “Gondwanan vicariance” hypothesis, cichlids lived on the Gondwanan landmasses South America, Africa, Madagascar, and India before the separation of these landmasses and diverged as a result of this separation. This would require cichlids to be at least as old as the initial Gondwanan split, i.e., 150 million years. The “Oceanic dispersal” hypothesis posits that cichlids are younger than the separation of Gondwanan landmasses and hence reached their current distributions through long-distance oceanic dispersal. Some molecular studies suggest that this could have occurred around 70 Ma. An alternative hypothesis that is consistent with a young age of cichlids is the “Independent colonization” scenario, according to which cichlids on all four landmasses independently evolved from a common marine ancestor that has since either gone extinct or remained undiscovered. This must have occurred before 45 Ma because the presence of freshwater cichlids by that time is well documented in the fossil record.

Fig. 2. The genomic timeline of cichlid and teleost diversification.

The 14 cichlid species with new genome sequences are highlighted in bold. Fossils used for time calibration are marked on branches according to the fossil’s age and its uncertainty. For seven clades, the first occurrence is ambiguous. In these cases, the younger and older of the two potential first records are marked in purple and red, respectively. One example of such a clade, Tetraodontiformes, is shown in the first inset. Either †Cretatriacanthus guidottii (89.8–83.0 Ma) or †Plectocretacicus clarae (100.3–98.0 Ma) represent the first record of this clade. Our new model for time calibration with ambiguous first records calculates separate CladeAge prior densities for both fossils (shown in purple and red) and forms a combined prior density (shown in dark gray) based on these. The resulting genomic age estimate (posterior; shown in light gray) indicates that Tetraodontiformes are younger than †Plectocretacicus and thus supports †Cretatriacanthus as the first record of the group. The CladeAge prior density for the oldest cichlid record, †Mahengechromis, and the age estimates for the four cichlid subfamilies are shown in the second inset. A version of this phylogeny with all tip labels is provided in Supplementary Fig. 6.