Repeated Evolution Versus Common Ancestry: Sex Chromosome Evolution in the Haplochromine CichlidPseudocrenilabrus philander

Abstract

Why sex chromosomes turn over and remain undifferentiated in some taxa, whereas they degenerate in others, is still an area of ongoing research. The recurrent occurrence of homologous and homomorphic sex chromosomes in distantly related taxa suggests their independent evolution or continued recombination since their first emergence. Fishes display a great diversity of sex-determining systems. Here, we focus on sex chromosome evolution in haplochromines, the most species-rich lineage of cichlid fishes. We investigate sex-specific signatures in the Pseudocrenilabrus philander species complex, which belongs to a haplochromine genus found in many river systems and ichthyogeographic regions in northern, eastern, central, and southern Africa. Using whole-genome sequencing and population genetic, phylogenetic, and read-coverage analyses, we show that one population of P. philander has an XX–XY sex-determining system on LG7 with a large region of suppressed recombination. However, in a second bottlenecked population, we did not find any sign of a sex chromosome. Interestingly, LG7 also carries an XX–XY system in the phylogenetically more derived Lake Malawi haplochromine cichlids. Although the genomic regions determining sex are the same in Lake Malawi cichlids and P. philander , we did not find evidence for shared ancestry, suggesting that LG7 evolved as sex chromosome at least twice in haplochromine cichlids. Hence, our work provides further evidence for the labile nature of sex determination in fishes and supports the hypothesis that the same genomic regions can repeatedly and rapidly be recruited as sex chromosomes in more distantly related lineages.

Dynamics of sex chromosome evolution in a rapid radiation of cichlid fishes

“…LG being a sex chromosome at this time derived from ancestral state reconstructions. and previously published summaries 25,26 .…”

“…1 , Supplementary Fig. 7), in several Lake Malawi cichlids 28,29 (Haplochromini), as well as in P. philander 25 (Haplochromini), making it the most widespread sex-linked LG known in cichlids to date.…”

“…LGs identified in at least one species as sex-linked, incorporating the published data for two labstrains and a cross derived from a natural population of A. burtoni 38,39 and a population of P. philander 25 (permissive dataset; stringent dataset 13 LGs). Note that P. philander was present in the current dataset with a single individual only and the A. burtoni samples included here derive from two different populations not allowing the confirmation of previously published data.…”

“…Here, we were interested if sex determination is keeping pace with other traits in cichlids by determining the diversity of SD systems and by investigating the dynamics of sex chromosome turnover across the entire LT cichlid radiation. The available data from about 30 African cichlid species (reviewed in 25,26 ) suggest that sex chromosomes are not conserved in this group with both simple and polygenic sex determination systems being known from the different species investigated. An emerging picture is that certain chromosomes have recurrently been recruited as sex chromosomes in cichlids.…”

Preface: advances in cichlid research III: behavior, ecology, and evolutionary biology

“…Fishes are known for their great variety of different sexdetermining systems. This is particularly true for African cichlid fishes, for which a stunning diversity of sex chromosomes and potential environmental sex determination have been documented (Gammerdinger & Kocher, 2018;Böhne et al 2019). Using whole genome data, Gammerdinger et al (2019) characterized and compared young sex chromosomes across three species of basal haplotilapiine tribes.…”