The Diversity and Evolution of Sex Chromosomes in Frogs

Abstract

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.

Why Do Some Vertebrates Have Microchromosomes?

“…Nevertheless, the rate of chromosomal rearrangements in amphibians was previously estimated to be less frequent compared to mammals [ 107 ]. Recent genomic studies have shown that chromosomes experienced high levels of fusion type rearrangements in salamanders and frog species [ 108 , 109 ]. Further studies are required to investigate whether this high-level tendency of chromosomal rearrangements in amphibian genomes can trigger the formation of microchromosomes, and how such forces might impact their evolution.…”

“…In addition to amniotes, other vertebrate genomes including some primitive amphibians and lower bony fish also represent a highly dynamic number of microchromosomes. The karyotypes of Cryptobranchidae and Hynobiidae families of amphibians can carry 2 n chromosomes ranging from 56–66, with 14–19 pairs of microchromosomes [ 11 , 69 ] Chromosomal linkage homologies, as well as fission and fusion rearrangements have been detected between avian and amphibian genomes, and comparative mapping showed a considerable amount of homology between different macro- and microchromosomes [ 109 , 288 ]. Microchromosomes can also be found in chondrostean and holostean fish (2 n = 46–112), related to crossopterygian fish that gave rise to terrestrial vertebrates 280 Mya, with genomes similar in size to birds [ 53 ].…”

Tempo of degeneration across independently evolved non-recombining regions

“…Recombination suppression evolved numerous times in a wide range of organisms, even sometimes within the same genus and at different times [56,57]. Moreover, the evolutionary strata present in some sex chromosomes represent stepwise extension events of recombination suppression that occurred at different time points; e.g., the four successive steps of recombination suppression on the mammalian Y chromosome [52,58,59].…”

“…However, a formal study of the tempo of degeneration requires data from a large number of independent events of recombination suppression of varying ages, which has not been available so far (Charlesworth 2021). Recombination suppression has however evolved numerous times in a wide range of organisms, even sometimes multiple independent times within the same genus (Ma and Veltsos 2021; Mrackova, et al 2008). Moreover, the evolutionary strata present in some sex chromosomes represent stepwise extension events of recombination suppression that occurred at different time points; e.g ., the four successive steps of recombination suppression on the mammalian Y chromosome (Lahn and Page 1999; Ross, et al 2009; Skaletsky, et al 2003).…”

A dense linkage map for a large repetitive genome: discovery of the sex-determining region in hybridizing fire-bellied toads (Bombina bombinaandBombina variegata)

“…As a first application of the new linkage map, we identified the sex determining (SD) region in Bombina , which together with the majority of amphibians lack heteromorphic sex chromosomes ( Eggert 2004 ; Ma and Veltsos 2021 ). Diplotype estimates were coupled with histological estimates of F2 progeny sex.…”