Patterns of genomic differentiation between two Lake Victoria cichlid species, Haplochromis pyrrhocephalus and H. sp. ‘macula’

Abstract

Background The molecular basis of the incipient stage of speciation is still poorly understood. Cichlid fish species in Lake Victoria are a prime example of recent speciation events and a suitable system to study the adaptation and reproductive isolation of species. Results Here, we report the pattern of genomic differentiation between two Lake Victoria cichlid species collected in sympatry, Haplochromis pyrrhocephalus and H. sp. ‘macula,’ based on the pooled genome sequences of 20 individuals of each species. Despite their ecological differences, population genomics analyses demonstrate that the two species are very close to a single panmictic population due to extensive gene flow. However, we identified 21 highly differentiated short genomic regions with fixed nucleotide differences. At least 15 of these regions contained genes with predicted roles in adaptation and reproductive isolation, such as visual adaptation, circadian clock, developmental processes, adaptation to hypoxia, and sexual selection. The nonsynonymous fixed differences in one of these genes, LWS , were reported as substitutions causing shift in absorption spectra of LWS pigments. Fixed differences were found in the promoter regions of four other differentially expressed genes, indicating that these substitutions may alter gene expression levels. Conclusions These diverged short genomic regions may have contributed to the differentiation of two ecologically different species. Moreover, the origins of adaptive variants within the differentiated regions predate the geological formation of Lake Victoria; thus Lake Victoria cichlid species diversified via selection on standing genetic variation. Electronic supplementary material The online version of this article (10.1186/s12862-019-1387-2) contains supplementary material, which is available to authorized users.

Genomic determinants of speciation

“…Genomic analysis of incipient species shows that divergence between them is frequently concentrated in certain genomic regions, termed "genomic islands of speciation" (Takuno et al 2019). Similarly, we set out to identify genes that have diverged rapidly between species but retained relatively low polymorphism within species, and consider them to be putative "speciation genes".…”

Phylogeography of high Andean killifishesOrestias(Teleostei: Cyprinodontidae) in Caquena and Lauca sub-basins of the Altiplano (Chile): mitochondrial and nuclear analysis of an endangered fish

“…This area is interesting to analyze evolutionary relations of Orestias, especially considering its geographical proximity to the proposed center of radiation of the genus and also, that given its rapid speciation characteristics and to the history of the geological, hydrological and climatic changes that have occurred in the Altiplano since its formation (Morales, Vila & Poulin, 2011). Differentiation processes linked to adaptation during short evolutionary periods has been evidenced in fishes of the Cichlidae family that inhabit Victoria Lake in Africa, or Apoyeque Lake in Nicaragua where a sympatry process could explain the high diversity of species within the same lake (Elmer et al, 2010;Takuno et al, 2019). Furthermore, some species of cichlids have shown similar morphological features (Kocher, 2004) where has been postulated a radiation of species related to colonization events by different lineages due to allopatry.…”

Ancient standing genetic variation facilitated the adaptive radiation of Lake Victoria cichlids

“…Therefore, this finding pointed to the possibility that the divergent alleles that might contribute to the adaptive radiation of Lake Victoria cichlids (14,600 years ago) had built up before the radiation of Lake Tanganyika cichlids (5-10 million years ago). Although more than a dozen genes with divergent alleles derived from SGV have been identified (Nikaido et al, 2014;Meier et al, 2017;Takuno et al, 2019;McGee et al, 2020;Urban et al, 2021), they might be only a small part of the genomic substrate that yielded cichlid radiation. Nevertheless, it had remained to be investigated which genes had large-scale SGV, such as the allelic diversity of V1R2, and to what extent largescale SGV accounted for the genetic factors driving rapid speciation and adaptation of East African cichlids.…”