Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards

Abstract

Distribution of sex-determining mechanisms across Australian agamids shows no clear phylogenetic segregation, suggesting multiple transitions between temperature-dependent (TSD) and genotypic sex determination (GSD). These taxa thus present an excellent opportunity for studying the evolution of sex chromosomes, and evolutionary transitions between TSD and GSD. Here we report the hybridization of a 3 kb genomic sequence (PvZW3) that marks the Z and W microchromosomes of the Australian central bearded dragon (Pogona vitticeps) to chromosomes of 12 species of Australian agamids from eight genera using fluorescence in-situ hybridization (FISH). The probe hybridized to a single microchromosome pair in 11 of these species, but to the tip of the long arm of chromosome pair 2 in the twelfth (Physignathus lesueurii), indicating a micro-macro chromosome rearrangement. Three TSD species shared the marked microchromosome, implying that it is a conserved autosome in related species that determine sex by temperature. C-banding identified the marked microchromosome as the heterochromatic W chromosome in two of the three GSD species. However, in Ctenophorus fordi, the probe hybridized to a different microchromosome from that shown by C-banding to be the heterochromatic W, suggesting an independent origin for the ZW chromosome pair in that species. Given the haphazard distribution of GSD and TSD in this group and the existence of at least two sets of sex microchromosomes in GSD species, we conclude that sex-determining mechanisms in this family have evolved independently, multiple times in a short evolutionary period.

Extension, single-locus conversion and physical mapping of sex chromosome sequences identify the Z microchromosome and pseudo-autosomal region in a dragon lizard, Pogona vitticeps

“…Indeed, we recently performed comparative FISH experiments using the amplified 3-kb fragment of contig C as a hybridization probe to deduce sex chromosome homology among 12 species of Australian agamids (Ezaz et al, 2009). This identified independent origins of ZZ/ ZW sex chromosome systems among GSD dragons and identified chromosomes in TSD dragons that are homologous to the sex chromosomes of P. vitticeps.…”

“…This is true even within the family of dragon lizards (Agamidae), which are emerging as a model group for the study of sex determination evolution, sex ratio evolution and sex allocation (Harlow, 2004;Ezaz et al, 2005;Warner and Shine, 2005;Doody et al, 2006;Janzen and Phillips, 2006;Quinn et al, 2007;Shine, 2007, 2008;Ezaz et al, 2009). They present an excellent opportunity to understand better the molecular and chromosomal basis of evolutionary transitions between the two fundamental mechanisms of vertebrate sex determination, TSD and GSD.…”

The Birds and the Bees and the Flowers and the Trees: Lessons from Genetic Mapping of Sex Determination in Plants and Animals

“…These inferences remain tentative, as there is no definitive reptile phylogeny (Olmo 2005;Pokorna and Kratochvil 2009). In the Australian dragon lizards, FISH mapping combined with phylogenetic analysis has demonstrated that female heterogametic sex determination evolved at least twice independently from temperature-sensitive ESD (Ezaz et al 2005(Ezaz et al , 2009. Separate sexes and GSD in birds probably evolved independently of the change to GSD in reptiles, since the reptile DMRT1 homolog is autosomal (Kawai et al 2007).…”

Foreword: sex and sex chromosomes—new clues from nonmodel species

“…Mammalian SRY may be nearing the end of its use by date, as demonstrated by two rodent groups that have dispensed with it in favor of as yet unknown substitutes in mole voles (Bagheri-Fam et al, this issue) and spiny rats (Murata et al, this issue). Clearly, there is evidence for many turnovers of the vertebrate sex chromosomes-and sex-determining genes, even among closely related species (Ezaz et al 2009a(Ezaz et al , b, 2010Mawaribuchi et al, this issue), and it is important to understand how one sex-determining gene can give way to another.…”