Dataset Information

The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis chilotes x H. nyererei).

ABSTRACT: The independent evolution of the two toothed jaws of cichlid fishes is thought to have promoted their unparalleled ecological divergence and species richness. However, dental divergence in cichlids could exhibit substantial genetic covariance and this could dictate how traits like tooth numbers evolve in different African Lakes and on their two jaws. To test this hypothesis, we used a hybrid mapping cross of two trophically divergent Lake Victoria species (Haplochromis chilotes × Haplochromis nyererei) to examine genomic regions associated with cichlid tooth diversity. Surprisingly, a similar genomic region was found to be associated with oral jaw tooth numbers in cichlids from both Lake Malawi and Lake Victoria. Likewise, this same genomic location was associated with variation in pharyngeal jaw tooth numbers. Similar relationships between tooth numbers on the two jaws in both our Victoria hybrid population and across the phylogenetic diversity of Malawi cichlids additionally suggests that tooth numbers on the two jaws of haplochromine cichlids might generally coevolve owing to shared genetic underpinnings. Integrated, rather than independent, genomic architectures could be key to the incomparable evolutionary divergence and convergence in cichlid tooth numbers.

SUBMITTER: Hulsey CD

PROVIDER: S-EPMC5592944 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Publications

The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis chilotes x H. nyererei).

Hulsey C Darrin CD Machado-Schiaffino Gonzalo G Keicher Lara L Ellis-Soto Diego D Henning Frederico F Meyer Axel A

G3 (Bethesda, Md.) 20170907 9

The independent evolution of the two toothed jaws of cichlid fishes is thought to have promoted their unparalleled ecological divergence and species richness. However, dental divergence in cichlids could exhibit substantial genetic covariance and this could dictate how traits like tooth numbers evolve in different African Lakes and on their two jaws. To test this hypothesis, we used a hybrid mapping cross of two trophically divergent Lake Victoria species (Haplochromis chilotes × Haplo ...[more]

PMID: 28751505

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Project description:BackgroundCichlids 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.ResultsOur 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.ConclusionsDivergence 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.

Project description:Divergence within cis-regulatory sequences may contribute to the adaptive evolution of gene expression, but functional alleles in these regions are difficult to identify without abundant genomic resources. Among African cichlid fishes, the differential expression of seven opsin genes has produced adaptive differences in visual sensitivity. Quantitative genetic analysis suggests that cis-regulatory alleles near the SWS2-LWS opsins may contribute to this variation. Here, we sequence BACs containing the opsin genes of two cichlids, Oreochromis niloticus and Metriaclima zebra. We use phylogenetic footprinting and shadowing to examine divergence in conserved non-coding elements, promoter sequences, and 3'-UTRs surrounding each opsin in search of candidate cis-regulatory sequences that influence cichlid opsin expression.We identified 20 conserved non-coding elements surrounding the opsins of cichlids and other teleosts, including one known enhancer and a retinal microRNA. Most conserved elements contained computationally-predicted binding sites that correspond to transcription factors that function in vertebrate opsin expression; O. niloticus and M. zebra were significantly divergent in two of these. Similarly, we found a large number of relevant transcription factor binding sites within each opsin's proximal promoter, and identified five opsins that were considerably divergent in both expression and the number of transcription factor binding sites shared between O. niloticus and M. zebra. We also found several microRNA target sites within the 3'-UTR of each opsin, including two 3'-UTRs that differ significantly between O. niloticus and M. zebra. Finally, we examined interspecific divergence among 18 phenotypically diverse cichlids from Lake Malawi for one conserved non-coding element, two 3'-UTRs, and five opsin proximal promoters. We found that all regions were highly conserved with some evidence of CRX transcription factor binding site turnover. We also found three SNPs within two opsin promoters and one non-coding element that had weak association with cichlid opsin expression.This study is the first to systematically search the opsins of cichlids for putative cis-regulatory sequences. Although many putative regulatory regions are highly conserved across a large number of phenotypically diverse cichlids, we found at least nine divergent sequences that could contribute to opsin expression differences in cis and stand out as candidates for future functional analyses.

Dataset Information

The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis chilotes x H. nyererei).

Publications

The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (<i>Haplochromis chilotes</i> x <i>H. nyererei</i>).

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