Diversity of Sex Chromosomes in Vertebrates: Six Novel Sex Chromosomes in Basal Haplochromines (Teleostei: Cichlidae)

Abstract

African cichlid fishes are known for their high rates of phenotypic evolution. A rapid rate of diversification is apparent also in the diversity of their sex chromosomes. To date, sex determiners have been identified on 18 of 22 chromosomes in the standard karyotype. Here, we use whole-genome sequencing to characterize the sex chromosomes of seven populations of basal haplochromines, focusing on the genus Pseudocrenilabrus. We identify six new sex chromosome systems, including the first report of a cichlid sex-determining system on linkage group 12. We then quantify the rates and patterns of sex chromosome turnover in this clade. Finally, we test whether some autosomes become sex chromosomes in East African cichlids more often than expected by chance.

Keywords: Pseudocrenilabrus; African cichlids; sex chromosome turnover.

Fig. 1.

Geographic context of the basal haplochromines. Map depicting approximate locations of rivers and lakes relevant to this study, adapted from Egger et al. (2015).

Fig. 2.

Differentiation between male and female P. philander “Thamalakane River.” The top panel plots F_ST-quantifying allele frequency differences between the male and female DNA pools. The middle panel shows the frequency of male-patterned (Y) alleles, and the bottom panel shows the frequency of female-patterned (W) alleles.

Fig. 3.

Whole-genome F_ST plots on the M. zebra UMD2a reference for a) P. philander “Lake Mweru,” b) P. multicolor victoriae, and c) P. multicolor multicolor.

Fig. 4.

Whole-genome F_ST plots on the M. zebra UMD2a reference for a) P. nicholsi, b) L. relictus, and c) T. callichromus.

Fig. 5.

Distribution of independent origins of sex chromosome on 23 chromosomes in East African cichlids and best fit of the data to a Poisson distribution with mean of 2.2 (χ² test, P = 0.246).

Fig. 6.

Sex chromosome turnovers in basal haplochromine cichlids in the context of adjacent groups. Topology is derived from Ronco et al. (2021) and Astudillo et al. (2023), with species not included in these studies incorporated according to their phylogenetic position and relative divergence times in other studies (Koblmüller, Schliewen, et al. 2008; Irisarri et al. 2018; Meier et al. 2019; Schedel et al. 2019). Blue indicates an XY system, red indicates a ZW system, and purple indicates the presence of both XY and ZW signal on the same chromosome.