Persistence of an unusual triple sex chromosome system through allopolyploidization in African clawed frogs (Xenopus, subgenus Silurana)

Abstract

African clawed frogs (Xenopus) have a high rate of genome duplication, which may catalyze evolution—including of sex chromosomes. To explore this, for each of four species in the subgenus Silurana, we analyzed sex-associated genetic variation, and in the diploid species X. tropicalis, we explored population structure. We found that the sex-linked regions in all four species are homologous, and we infer that X. calcaratus has an unusual sex determination system with three sex chromosomes, which was previously known only in X. tropicalis. Our results evidence two independent allotetraploidization in Silurana, admixture across ploidy levels, and demonstrate that the most recent allotetraploidization that generated the X. calcaratus lineage occurred after population subdivision arose in X. tropicalis. Thus, this unusual triple sex chromosome system has been maintained independently in two different species for a protracted period and through an allotetraploidization event. Simulations indicate that genetic drift should eliminate one of the sex chromosomes, suggesting that there may be unidentified benefits to maintaining this complex system.