The Sex Chromosomes of Frogs: Variability and Tolerance Offer Clues to Genome Evolution and Function

Abstract

Frog sex chromosomes offer an ideal system for advancing our understanding of genome evolution and function because of the variety of sex determination systems in the group, the diversity of sex chromosome maturation states, the ease of experimental manipulation during early development. After briefly reviewing sex chromosome biology generally, we focus on what is known about frog sex determination, sex chromosome evolution, and recent, genomics-facilitated advances in the field. In closing we highlight gaps in our current knowledge of frog sex chromosomes, and suggest priorities for future research that can advance broad knowledge of gene dose and sex chromosome evolution.

Did sex chromosome turnover promote divergence of the major mammal groups?

“…In sticklebacks, too, novel sex genes have rapidly arisen 18, 19, and in cichlid fish of Lake Victoria, rampant speciation is often accompanied by sex chromosome turnover 20. In frogs, too, different sex determining genes and sex chromosome systems have arisen, and one species is polymorphic for XY and ZW systems 21, 22, 23, 24.…”

Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma

“…Low, or suppressed, recombination leads to a reduction in effective population size (N e ) through selection at linked sites; thereby the efficacy of selection is reduced and we expect an increased mutational load (Bachtrog and Charlesworth 2002;Charlesworth and Charlesworth 2010). The link between recombination suppression and molecular degeneration has been observed in the sex-and mating-type determining genomic regions of a number of taxa across all eukaryote kingdoms (e.g., Bachtrog 2003;Hood et al 2004;Liu et al 2004;Marais et al 2008;Whittle and Johannesson 2011;Whittle et al 2011a;Fontanillas et al 2015) and is one of the main factors expected to favor either rare recombination events on sex chromosomes (Malcom et al 2014) or a high turnover of chromosomes harboring the sex-determining loci (Blaser et al 2013). …”

Evidence for Sex Chromosome Turnover in Proteid Salamanders

“…Remarkably, despite a constitutive embryonic mortality rate of 50% (and possible skewed sex ratio [Wallace, 1984]), this balanced lethal heterozygosity has withstood millions of years of evolution, including at least 5 speciation events [Sessions et al, 1988;Macgregor et al, 1990]! If our interpretation is correct, then Proteus provides an important example of sex chromosome turnover, reflecting a general trend in amphibians, identified by Malcolm et al [2014], for the transformation of heteromorphic to homomorphic sex chromosomes. Two alternative models for such a trend have been suggested: the 'Fountain of Youth Model' and the 'High Turnover Model' [Perrin, 2009;Stöck et al, 2011;Malcolm et al, 2014].…”

“…However, recent evidence suggests that underlying sex determination mechanisms in amphibians appear to be extraordinarily labile [Hillis and Green, 1990;Evans et al, 2012;Graves, 2013], and transformations from WZ to XY or vice versa, sometimes involving reversals from heteromorphic to homomorphic sex chromosomes, may be surprisingly common and rapid [Landeen and Presgraves, 2013;Miura and Ogata, 2013;Blaser et al, 2014;Dufresnes et al, 2015]. Exactly how such changes come about is not fully understood, but it may involve genetic problems associated with dosage compensation and genome balance, as well as the maintenance of stable sex ratios [Malcolm et al, 2014]. Although the role of certain epigenetic factors, especially temperature, has been mentioned as a possible factor in destabilizing sex determination in amphibians under extreme conditions [Wallace, 1984;Eggert, 2004;Grossen et al, 2012;van Doorn, 2014], there is no documented case of temperature-controlled sex determination in amphibians, and sex determination is probably genetically controlled in all amphibians regardless of whether they have heteromorphic or homomorphic sex chromosomes [Hillis and Green, 1990;Hayes, 1998].…”

“…The elimination of heteromorphic sex chromosomes in favor of homomorphic sex chromosomes may also be important in the maintenance of genetic diversity [Perrin, 2009]. These changes sometimes involve recombination between the sex chromosomes and autosomes, or between the sex chromosomes themselves [Malcolm et al, 2014].…”