Differential use of multiple genetic sex determination systems in divergent ecomorphs of an African crater lake cichlid

Abstract

African cichlid fishes not only exhibit remarkably high rates of speciation but also have some of the fastest evolving sex determination systems in vertebrates. However, little is known empirically in cichlids about the genetic mechanisms generating new sex-determining variants, what forces dictate their fate, the demographic scales at which they evolve, and whether they are related to speciation. To address these questions, we looked for sex-associated loci in full genome data from 647 individuals of Astatotilapia calliptera from Lake Masoko, a small isolated crater lake in Tanzania, which contains two distinct ecomorphs of the species. We identified three separate XY systems on recombining chromosomes. Two Y alleles derive from mutations that increase expression of the gonadal soma-derived factor gene (gsdf) on chromosome 7; the first is a tandem duplication of the entire gene observed throughout much of the Lake Malawi haplochromine cichlid radiation to which A. calliptera belongs, and the second is a 5 kb insertion directly upstream of gsdf. Both the latter variant and another 700 bp insertion on chromosome 19 responsible for the third Y allele arose from transposable element insertions. Males belonging to the Masoko deep-water benthic ecomorph are determined exclusively by the gsdf duplication, whereas all three Y alleles are used in the Masoko littoral ecomorph, in which they appear to act antagonistically among males with different amounts of benthic admixture. This antagonism in the face of ongoing admixture may be important for sustaining multifactorial sex determination in Lake Masoko. In addition to identifying the molecular basis of three coexisting sex determining alleles, these results demonstrate that genetic interactions between Y alleles and genetic background can potentially affect fitness and adaptive evolution.

Genomics of cold adaptations in the Antarctic notothenioid fish radiation

“…Transposable element dynamics are increasingly recognised as major drivers of evolutionary innovation, and their analysis is greatly facilitated by the use of long-read sequencing technologies 41,42 . For example, the location of TE insertions can influence the expression of nearby genes and induce phenotypic variation 43,44 . The diversity of transposons varies substantially between organisms, with teleost fish genomes containing greater TE diversity compared to other vertebrates, such as mammals 41,45 .…”

Taming transposable elements in vertebrates: from epigenetic silencing to domestication

“…In fact, recent evidence suggests that TEs have contributed further to the astonishing ecomorphological diversity of East African cichlids. Two recent studies have identified insertions of DNA TEs and retrotransposons close to opsin genes and to gsdf, with potentially important consequences for visual and sex determination systems, respectively [88,89]. It is appealing to contemplate TE-derived cis-regulatory activity driving or fueling adaptive radiation, in lieu of low genetic diversity.…”

Oca2targeting using CRISPR/Cas9 in the Malawi cichlidAstatotilapia calliptera

“…Using such an approach, several studies identified genes associated with interspecific variation in craniofacial profiles, jaw attributes, colour patterns and sex determination systems. The increase in genomic resources and the low costs of whole genome sequencing are also leading to an increase in genome-wide association studies in wild populations giving unprecedented insights into intraspecific variation [57,59]. A commonality between all these studies is that often the causal variants are in non-coding regions, hence establishing methods to edit non-coding regions will facilitate the dissection of their functional role.…”