A rapid rate of sex-chromosome turnover and non-random transitions in true frogs

Abstract

The canonical model of sex-chromosome evolution predicts that, as recombination is suppressed along sex chromosomes, gametologs will progressively differentiate, eventually becoming heteromorphic. However, there are numerous examples of homomorphic sex chromosomes across the tree of life. This homomorphy has been suggested to result from frequent sex-chromosome turnovers, yet we know little about which forces drive them. Here, we describe an extremely fast rate of turnover among 28 species of Ranidae. Transitions are not random, but converge on several chromosomes, potentially due to genes they harbour. Transitions also preserve the ancestral pattern of male heterogamety, in line with the 'hot-potato' model of sex-chromosome transitions, suggesting a key role for mutation-load accumulation in non-recombining genomic regions. The importance of mutation-load selection in frogs might result from the extreme heterochiasmy they exhibit, making frog sex chromosomes differentiate immediately from emergence and across their entire length.

Fig. 1

Sex chromosome turnovers across 28 true frog species. Sex-determination system and sex-chromosome identities come from both RADseq (Supplementary Table 1) and literature (Supplementary Table 2) data. Karyotype (top left, chromosomes not to scale) shows the number of species using each chromosome for sex determination and colours correspond to arrows, node pie charts and tips. Coloured arrows show the branch on which inferred turnovers occur based on the stochastic mapping analyses (Supplementary Fig. 8) and the pie charts at nodes represent the proportion of simulated trees in stochastic mapping with each of the states at that node. Tips with two colours represent intraspecific turnover events, with the transition described by the coloured arrow after the species name. Grey represents unknown sex chromosome identities in both tips and turnover arrows 1 and 2 and question marks at tips represent an unknown system of heterogamety. As there was not enough high-quality sequence information for P. porosus, it could not be included in the phylogenetic reconstruction or stochastic mapping. Its position here is inferred from that in ref.

Fig. 2

Non-random recruitment of chromosomes for sex determination. Grey bars represent the number of genes per X. tropicalis chromosome. Violin plots show the expected number of times each chromosome would be recruited if genes were recruited for sex determination at random (1000 replicates). Black dots represent the number of times each chromosome was observed as recruited from our data

Fig. 3

Chromosome-wide distribution of sex-linked RAD markers in seven true frog species. Density plots to the left of linkage maps show the marker density along the linkage group. Coloured bars are histograms of the number of sex-linked markers along the linkage group, with bins of 2 cM. Picture credits: Jan Jezek (R. arvalis), Astolinto (R. italica), Yasunori Koide (R. japonica), Jim Rorabaugh (R. montezumae), DLJ (R. iberica), NR (R. dalmatina), AB (R. kukunoris)