Sequential Turnovers of Sex Chromosomes in African Clawed Frogs (Xenopus) Suggest Some Genomic Regions Are Good at Sex Determination

Abstract

Sexual differentiation is fundamentally important for reproduction, yet the genetic triggers of this developmental process can vary, even between closely related species. Recent studies have uncovered, for example, variation in the genetic triggers for sexual differentiation within and between species of African clawed frogs (genus Xenopus). Here, we extend these discoveries by demonstrating that yet another sex determination system exists in Xenopus, specifically in the species Xenopus borealis. This system evolved recently in an ancestor of X. borealis that had the same sex determination system as X. laevis, a system which itself is newly evolved. Strikingly, the genomic region carrying the sex determination factor in X. borealis is homologous to that of therian mammals, including humans. Our results offer insights into how the genetic underpinnings of conserved phenotypes evolve, and suggest an important role for cooption of genetic building blocks with conserved developmental roles.

Divergent subgenome evolution after allopolyploidization in African clawed frogs (Xenopus)

“…Sequence data analysed in this study were obtained from a recent phylogenetic analysis of Xenopus (Furman & Evans, ). The dataset was generated from a total of six species (one diploid, five allotetraploids), including previously published RNASeq data from four Xenopus ( X. borealis , X. clivii , X. largeni , and X. allofraseri ) and downloaded Unigene libraries from X. laevis and Xenopus Silurana tropicalis (Unigene database, last modified March 2013).…”

“…To generate a starting tree topology, we used RAxML v.8.2.4 (Stamatakis, ) and set a GTRGAMMA model, followed by 500 bootstrap replicates to assess support. Strongly supported nodes are consistent with the phylogenetic analyses of Furman & Evans (), but include different relationships among X. laevis , X. allofraseri and X. largeni between the L‐lineage compared to the S‐lineage. This is due to poorly supported, short internal branch lengths and a lower mutation rate of the L‐subgenome (Fig.…”

“…Each of these allotetraploid species have two subgenomes of nine homologous chromosome pairs each (the ‘L’ and the ‘S’ subgenome; Matsuda et al ., ) that were inherited from different diploid ancestral species that generated the shared allotetraploid ancestor. Extensive multigene sequencing, genome analyses and cytogenetic work have demonstrated closer intraspecific relationships than interspecific for the two subgenomes, supporting the hypothesis that one allotetraploidization event between two diploid progenitor lineages gave rise to the extant Xenopus allotetraploids (Tymowska, ; Evans et al ., , ; Furman & Evans, ; Session et al ., ). Other scenarios are possible, for example, supplementary information of Bewick et al ., ; but one allotetraploidization event is the most parsimonious scenario.…”

Sex chromosome turnovers and genetic drift: a simulation study

“…Thanks to recent advances in genomic technologies, sex chromosome systems are now characterized across a wide range of nonmodel organisms, revealing that many clades experience frequent sex chromosome turnovers, whereby an ‘emergent’ mutant sex determiner replaces the ‘resident’ sex determiner at the top of the sex‐determining cascade. This is the case for instance in fishes (Mank & Avise, ), reptiles (Ezaz et al ., ), amphibians (Miura, ; Dufresnes et al ., ; Furman & Evans, ), Diptera (Vicoso & Bachtrog, ), isopods (Becking et al ., ) and Salicaceae (Muyle et al ., ).…”

Sex Determination and Sex Chromosomes in Amphibia

“…Chromosome 7 of Xenopus tropicalis , which is homologous to chromosome 9 in the frogs described above, is a homomorphic sex chromosome of female heterogamety . In addition, a X. borealis chromosome homologous to chromosome 7 in the abovedescribed frogs is a homomorphic sex chromosome of female heterogamety [Furman et al, 2016]. Further, the heteromorphic sex chromosomes of female heterogamety in 4 species of the genus Pseudis (Hylinae) might be homologous to chromosome 7 or 9 in the frogs described above [Busin et al, 2008].…”