Sex reversal triggers the rapid transition from genetic to temperature-dependent sex

• Published in: Nature (London) Vol. 523; no. 7558; pp. 79 - 82
• Main Authors: Holleley, Clare E., O'Meally, Denis, Sarre, Stephen D., Marshall Graves, Jennifer A., Ezaz, Tariq, Matsubara, Kazumi, Azad, Bhumika, Zhang, Xiuwen, Georges, Arthur
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 02-07-2015; Nature Publishing Group
• Subjects: 45; 45/22; 45/77; 631/181/2468; 631/181/2474; 631/208/182; Adaptation, Physiological; Animals; Australia; Female; Humanities and Social Sciences; letter; Male; Methods; Molecular Sequence Data; multidisciplinary; Reptiles; Science; Sex Chromosomes - genetics; Sex Determination Processes - genetics; Sex Determination Processes - physiology; Sex Ratio; Sex recognition (Zoology); Temperature; Australia
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature14574

The first report of reptile sex reversal in the wild and rapid transition between genetic and environmental sex determination in the Australian bearded dragon (
Pogona vitticeps
)
Climate-induced sex reversal
There have been repeated evolutionary transitions in reptiles between genetic and temperature-dependent sex determination, the regulatory process that initiates differentiation of the gonads in the early embryo to form either testes or ovaries. Various mechanisms have been proposed to explain the transition, including a role for sex reversal. Clare Holleley
et al
. present the first report of reptile sex reversal in the wild, associated with rapid transition between genetic and environmental sex determination. In a study of the Australian bearded dragon (
Pogona vitticeps
), they observe sex reversal at the warmer end of the animals geographic range. When sex-reversed females mate with normal males, the chromosomal sex determination system is lost and temperature-dependent sex determination is established. It is not known whether climate-induced changes in sex determination are advantageous or detrimental to the process of evolutionary adaptation.
Sex determination in animals is amazingly plastic. Vertebrates display contrasting strategies ranging from complete genetic control of sex (genotypic sex determination) to environmentally determined sex (for example, temperature-dependent sex determination)
1
. Phylogenetic analyses suggest frequent evolutionary transitions between genotypic and temperature-dependent sex determination in environmentally sensitive lineages, including reptiles
2
. These transitions are thought to involve a genotypic system becoming sensitive to temperature, with sex determined by gene–environment interactions
3
. Most mechanistic models of transitions invoke a role for sex reversal
3
,
4
,
5
. Sex reversal has not yet been demonstrated in nature for any amniote, although it occurs in fish
6
and rarely in amphibians
7
,
8
. Here we make the first report of reptile sex reversal in the wild, in the Australian bearded dragon (
Pogona vitticeps
), and use sex-reversed animals to experimentally induce a rapid transition from genotypic to temperature-dependent sex determination. Controlled mating of normal males to sex-reversed females produces viable and fertile offspring whose phenotypic sex is determined solely by temperature (temperature-dependent sex determination). The W sex chromosome is eliminated from this lineage in the first generation. The instantaneous creation of a lineage of ZZ temperature-sensitive animals reveals a novel, climate-induced pathway for the rapid transition between genetic and temperature-dependent sex determination, and adds to concern about adaptation to rapid global climate change.