East African cichlid lineages (Teleostei: Cichlidae) might be older than their ancient host lakes: new divergence estimates for the east African cichlid radiation

Abstract

Background Cichlids are a prime model system in evolutionary research and several of the most prominent examples of adaptive radiations are found in the East African Lakes Tanganyika, Malawi and Victoria, all part of the East African cichlid radiation (EAR). In the past, great effort has been invested in reconstructing the evolutionary and biogeographic history of cichlids (Teleostei: Cichlidae). In this study, we present new divergence age estimates for the major cichlid lineages with the main focus on the EAR based on a dataset encompassing representative taxa of almost all recognized cichlid tribes and ten mitochondrial protein genes. We have thoroughly re-evaluated both fossil and geological calibration points, and we included the recently described fossil † Tugenchromis pickfordi in the cichlid divergence age estimates. Results Our results estimate the origin of the EAR to Late Eocene/Early Oligocene (28.71 Ma; 95% HPD: 24.43–33.15 Ma). More importantly divergence ages of the most recent common ancestor (MRCA) of several Tanganyika cichlid tribes were estimated to be substantially older than the oldest estimated maximum age of the Lake Tanganyika: Trematocarini (16.13 Ma, 95% HPD: 11.89–20.46 Ma), Bathybatini (20.62 Ma, 95% HPD: 16.88–25.34 Ma), Lamprologini (15.27 Ma; 95% HPD: 12.23–18.49 Ma). The divergence age of the crown haplochromine H-lineage is estimated to 22.8 Ma (95% HPD: 14.40–26.32 Ma) and of the Lake Malawi radiation to 4.07 Ma (95% HDP: 2.93–5.26 Ma). In addition, we recovered a novel lineage within the Lamprologini tribe encompassing only Lamprologus of the lower and central Congo drainage with its divergence estimated to the Late Miocene or early Pliocene. Furthermore we recovered two novel mitochondrial haplotype lineages within the Haplochromini tribe: ‘ Orthochromis ’ indermauri and ‘ Haplochormis ’ vanheusdeni. Conclusions Divergence time estimates of the MRCA of several Tanganyika cichlid tribes predate the age of the extant Lake Tanganyika basin, and hence are in line with the recently formulated “Melting-Pot Tanganyika” hypothesis. The radiation of the ‘Lower Congo Lamprologus clade’ might be linked with the Pliocene origin of the modern lower Congo rapids as has been shown for other Lower Congo cichlid assemblages. Finally, the age of origin of the Lake Malawi cichlid flock agrees well with the oldest age estimate for lacustrine conditions in Lake Malawi. Electronic supplementary material The online version of this article (10.1186/s12862-019-1417-0) contains supplementary material, which is available to authorized users.

Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon

“…The visual opsin genes of the Barombi Mbo cichlids show very little variation at the nucleotide level (Table ), corresponding to the estimated geological age of current lake Barombi Mbo of less than 1 million years (Cornen et al, ) and the molecular dating of the onset of the Barombi Mbo radiation (around 1.7 million years ago ± 0.6 million years ago; Schedel, Musilova, & Schliewen, ). We observed between two and 15 haplotypes per gene (corresponding to 2–5 protein versions), whereby haplotypes are usually shared between species (Figure , Table ).…”

New haplochromine cichlid from the upper Miocene (9–10 MYA) of Central Kenya

“…The tribe can be subdivided into several lineages, of which the flock found in Lake Victoria and the neighbouring lakes (Edward, George and Kivu) is considered to be a superflock [26] ( Fig. 1b; see also [17] and [27]). In addition, all Haplochromini are maternal mouthbrooders and have evolved numerous specialized adaptations and feeding strategies (e.g., [28][29][30]).…”

“…One theory postulates that the Haplochromini originated within Lake Tanganyika, presumably about 5-6 MYA [25,45]. The other suggests that the emergence of the tribe predates the formation of Lake Tanganyika (the 'melting pot Tanganyika' hypothesis of Weiss et al [46]) and that their divergence age could be as old as 17 MYA (see [17] and Fig. 1b).…”

“…This second hypothesis is compatible with the proposal that at least Fig. 1 a Simplified composite phylogenetic tree depicting possible relationships among the Pseudocrenilabrinae, based on Schwarzer et al [14] and Dunz and Schliewen [15] (reused with slight modifications from Altner et al, [16] (open access article distributed under CC-BY-NC-ND 4.0 license; https://creativecommons.org/licenses/by-nc-nd/4.0/)); b Time calibrated phylogeny of all lineages comprising the Lake Tanganyika Radiation (re-drawn after Schedel et al, [17] distributed under CC-BY license (https://creativecommons.org/licenses/by/4.0/), simplified, error bars for ages of nodes not shown). The area of each triangle corresponds to the number of species used in the original publication; all lineages of the Haplochromini are depicted in green four different riverine lineages of Haplochromini (Tropheini, Pseudocrenilabrus, Astatoreochromis, and Astatotilapia) have independently colonized Lake Tanganyika (see [11]).…”

“…The area of each triangle corresponds to the number of species used in the original publication; all lineages of the Haplochromini are depicted in green four different riverine lineages of Haplochromini (Tropheini, Pseudocrenilabrus, Astatoreochromis, and Astatotilapia) have independently colonized Lake Tanganyika (see [11]). In addition, the phylogenetic reconstruction by Schedel et al [17] shows that the closest extant relatives of the Haplochromini all live in habitats that lie to the east of Lake Tanganyika: Four species of the paraphyletic genus Orthochromis, which are sister to the Haplochromini, thrive in the Malagarasi river system, while Ctenochromis pectoralis, which is sister to the remaining Haplochromini, is endemic to drainage systems in Kenya and Tanzania (see Fig. 1b).…”