Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

Abstract

The adaptive radiation of cichlid fishes in East Afrian Lake Malawi encompasses over 500 species that are believed to have evolved within the last 800 thousand years from a common founder population. It has been proposed that hybridisation between ancestral lineages can provide the genetic raw material to fuel such exceptionally high diversification rates, and evidence for this has recently been presented for the Lake Victoria Region cichlid superflock.Here we report that Lake Malawi cichlid genomes also show evidence of hybridisation between two lineages that split 3-4 million years ago, today represented by Lake Victoria cichlids and the riverine Astatotilapia sp. 'ruaha blue'. The two ancestries in Malawi cichlid genomes are present in large blocks of several kilobases, but there is little variation in this pattern between Malawi cichlid species, suggesting that the large-scale mosaic structure of the genomes was largely established prior to the radiation. Nevertheless, tens of thousands of polymorphic variants apparently derived from the hybridisation are interspersed in the genomes. These loci show a striking excess of differentiation across ecological subgroups in the Lake Malawi cichlid assemblage, and parental alleles sort differentially into benthic and pelagic Malawi cichlid lineages, consistent with strong differential selection on these loci during species divergence. Furthermore, these loci are enriched for genes involved in immune response and vision, including opsin genes previously identified as important for speciation. Our results reinforce the role of ancestral hybridisation in explosive diversification by demonstrating its significance in one of the largest recent vertebrate adaptive radiations.Recent advances in genome sequencing have provided empirical evidence that ancestral hybridisation can occur prior to adaptive radiation (Barrier et al. 1999) and can generate phenotypic novelty (Stryjewski and Sorenson 2017) . A group of species that has received considerable attention with

Movement of transposable elements contributes to cichlid diversity

“…We also searched newly sequenced genomes of 103 (Robinson et al, 2011;Thorvaldsdottir et al, 2013). Finally, we searched 53 additional genomes including 15 species from Lake Malawi, four from LVRS, four from Lake Tanganyika and 30 outgroups (Malinsky et al, 2018;McGee et al, 2015;Svardal et al, 2020). For these taxa, (Table S1).…”

“…These average allelic divergences were put into context by calculating their ratio either to the average sequence divergence between the deepest lineages within Lake Malawi (AlleleDiv/LM) or the sequence divergence for Lake Malawi and Victoria species (AlleleDiv/ MV (Malinsky et al, 2018). The genome sequence divergence for Malawi lineages compared to P. nyererei in Lake Victoria is ~0.0076 (Svardal et al, 2020). By comparing the allelic divergence at each locus to these two calibrations, we can determine if the alleles arose relatively recently (AlleleDiv/LM < 1), around the emergence of the Malawi lineages (AlleleDiv/LM ~ 1) or before the Malawi flock (AlleleDiv/ LM > 1 and AlleleDiv/MV ~ 0.5-1).…”

“…Questions of evolutionary predictability have focused on whether new phenotypes result from changes in coding sequence or gene regulation (Carroll, 2008;Hoekstra & Coyne, 2007;Stern & Orgogozo, 2008). In addition, there has been a strong focus on single nucleotide polymorphisms (SNPs) during the search for highly selected regions, magic genes, and islands of speciation (Malinsky et al, 2015(Malinsky et al, , 2018Servedio et al, 2011;Svardal et al, 2020;Turner & Hahn, 2010). However, evolution occurs through more than changes to single DNA bases.…”

Movement of transposable elements contributes to cichlid diversity

“…Introgression and hybridization have been demonstrated for cichlids in several African lakes (Salzburger et al 2002, Smith et al 2003, Meier et al 2017, Malinsky et al 2018, Svardal et al 2019). Therefore, past hybridization events within Lake Malawi cichlids might contribute to the increase in TEs within this flock, some of which could contribute to the genetic and phenotypic diversity we find here.…”

“…Questions of evolutionary predictability have focused on whether new phenotypes result from changes in coding sequence or gene regulation (Hoekstra and Coyne 2007, Carroll 2008, Stern and Orgogozo 2008. In addition, there has been a strong focus on single nucleotide polymorphisms (SNPs) during the search for highly selected regions, magic genes, and islands of speciation (Turner and Hahn 2010, Servedio et al 2011, Malinsky et al 2015, Malinsky et al 2018, Svardal et al 2019). However, evolution likely occurs through more than changes to single DNA bases.…”