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Molecular Marker Suggests Rapid Changes of Sex-Determining Mechanisms in Australian Dragon Lizards

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Molecular Marker Suggests Rapid Changes of Sex-Determining Mechanisms in Australian Dragon Lizards Chromosome Research (2009) 17:91–98 DOI 10.1007/s10577-008-9019-5 Molecular marker suggests rapid changes of sex-determining mechanisms in Australian dragon lizards Tariq Ezaz & Alexander E. Quinn & Stephen D. Sarre & Denis O’Meally & Arthur Georges & Jennifer A. Marshall Graves Received: 23 October 2008 /Revised and Accepted: 14 November 2008 / Published online: 27 January 2009 # Springer Science + Business Media B.V. 2009 Abstract Distribution of sex-determining mecha- micro-macro chromosome rearrangement. Three nisms across Australian agamids shows no clear TSD species shared the marked microchromosome, phylogenetic segregation, suggesting multiple transi- implying that it is a conserved autosome in related tions between temperature-dependent (TSD) and species that determine sex by temperature. C-banding genotypic sex determination (GSD). These taxa thus identified the marked microchromosome as the present an excellent opportunity for studying the heterochromatic W chromosome in two of the three evolution of sex chromosomes, and evolutionary GSD species. However, in Ctenophorus fordi, the transitions between TSD and GSD. Here we report probe hybridized to a different microchromosome the hybridization of a 3 kb genomic sequence from that shown by C-banding to be the heterochro- (PvZW3) that marks the Z and W microchromosomes matic W, suggesting an independent origin for the of the Australian central bearded dragon (Pogona ZW chromosome pair in that species. Given the vitticeps) to chromosomes of 12 species of Australian haphazard distribution of GSD and TSD in this group agamids from eight genera using fluorescence in-situ and the existence of at least two sets of sex micro- hybridization (FISH). The probe hybridized to a chromosomes in GSD species, we conclude that sex- single microchromosome pair in 11 of these species, determining mechanisms in this family have evolved but to the tip of the long arm of chromosome pair 2 in independently, multiple times in a short evolutionary the twelfth (Physignathus lesueurii), indicating a period. Keywords GSD . TSD . reptile . sex microchromosomes . evolution . FISH . C-banding Responsible Editor: Herbert Macgregor. Abbreviations T. Ezaz : D. O’Meally : J. A. Marshall Graves DAPI 4′,6-diamidino-2-phenylindole Comparative Genomics Group, Research School of dUTP 2′-deoxyuridine 5′-triphosphate Biological Sciences, The Australian National University, ESD environmental sex determination GPO Box 475, Canberra ACT 2601, Australia FISH fluorescence in-situ hybridization T. Ezaz (*) : A. E. Quinn : S. D. Sarre : A. Georges GSD genotypic sex determination Wildlife Genetics Laboratory, PCR polymerase chain reaction Institute for Applied Ecology, SSC standard saline citrate University of Canberra, Building 3, Canberra ACT 2601, Australia TSD temperature sex determination e-mail: [email protected] v/v volume/volume 92 T. Ezaz et al. Introduction to autosomes in three species of snakes and in the soft-shelled turtle Pelodiscus sinensis, indicating that Sex can be determined by genetic factors (genotypic the ZW sex chromosomes of birds are not homolo- sex determination, GSD), environmental factors (en- gous with the ZW macrochromosome pair common to vironmental sex determination, ESD) (Charnier 1966; all snakes or with the ZW microchromosomes of this Pieau 1971; Bull 1983), and in some cases, by an turtle (Matsubara et al. 2006; Kawai et al. 2007). interaction between genotype and environment (Con- However, Kawai et al. (2008) showed that in a ZW over and Kynard 1981; Quinn et al. 2007; Radder et population of the gecko Gekko hokouensis, the Z al. 2008). In many vertebrates, a primary sex- chromosome shares six genes with the chicken Z, determining gene on a specific chromosome pair raising the possibility of a bird-like ZW system in an (the sex chromosomes) provides the initial trigger for ancient reptile. It appears that different ancestral sex determination (Sinclair et al. 1990; Matsuda et al. autosomes gave rise to the sex chromosomes of 2002), whereas in other vertebrates, sex determination snakes and of Pelodiscus sinensis from the pair that depends on an environmental variable experienced became the bird and G. hokouensis ZW. during embryonic development, such as temperature, The only reports of lizard sex chromosome sequen- pH or salinity (Charnier 1966; Pieau 1971; Devlin ces include the six genes mapped in a gecko by Kawai et and Nagahama 2002). al. (2008), an X-linked microsatellite in Australian GSD vertebrates typically have either a male skinks (Cooper et al. 1997;Stowetal.2001), a W heterogametic (XY male/XX female) or a female chromosome sequence from the Asian varanid Varanus heterogametic (ZZ male/ZW female) sex chromosom- komodoensis (Halverson and Spelman 2002), a Y al system. The sex homologues (X and Y, or Z and chromosome sequence in the Australian skink W) may be highly differentiated, or differ only in a Bassiana duperreyi (unpublished observations) and restricted region (even a single locus), as is expected sequences common to the Z and W microchromo- given their autosomal origin. The XX/XY sex somes of the Australian bearded dragon lizard, Pogona chromosome pair is conserved in therian mammals, vitticeps (Agamidae) (Quinn et al. 2007). Substantial and a ZZ/ZW pair is conserved in birds. In contrast, sex chromosome sequence data have already started to many reptile, amphibian and fish lineages exhibit emerge from the genome sequencing project for the remarkable variation in the sex chromosome pair, and green anole lizard, Anolis carolinensis (http://www. in the system of heterogamety, sometimes even broad.mit.edu/models/anole/). among closely related species or even populations Two groups (Janzen and Krenz 2004; Organ and (for review see Ezaz et al. 2006; Graves 2006). Most Janes 2008) have recently reconstructed the evolu- turtles, a minority of lizards, all crocodilians and the tionary history of TSD and GSD within the Reptilia tuatara exhibit temperature-dependent sex determina- by mapping the occurrence of these mechanisms onto tion (TSD), in which incubation temperature during the phylogeny. Both groups considered GSD to be the egg development determines sex. GSD appears to be most parsimonious ancestral condition for squamate exhibited by all snakes, most lizards and a minority of reptiles (lizards and snakes). However, this conclusion turtles (Modi and Crews 2005; Ezaz et al. 2006), should be treated cautiously because GSD and TSD involving either male or female heterogamety (Solari may be omnibus states that (a) obscure diversity in 1994). Some lizards and snakes display more com- underlying mechanisms and so fail to separate plex male or female heterogametic systems involving convergence from homology; (b) are labile and multiple sex chromosomes in varying evolutionary therefore subject to frequent reversals that render stages of differentiation. parsimony a blunt instrument; and (c) include some Comparative mapping of sex chromosomal genes questionable classifications of TSD versus GSD (see or sequences across phylogenetically distinct taxa by Harlow 2004). In the absence of robust data on sex- fluorescence in-situ hybridization can provide valu- determining mechanisms from sufficient representa- able information on the origin and evolution of sex tive taxa, a complementary approach to determining chromosomes and sex-determining mechanisms. Re- ancestry of sex-determining mechanisms is compara- cently, orthologues of chicken Z genes were mapped tive mapping of sex chromosome sequences over a Multiple evolution of sex-determining mechanisms in dragon lizards 93 shorter evolutionary timescale within appropriate Materials and methods reptilian lineages. Dragon lizards (family Agamidae) include both Animals, sexing, cell culture, chromosome GSD and TSD taxa (Charnier 1966;Ganeshand preparations Raman 1995; Harlow and Shine 1999;Harlow2000, 2004; Harlow and Taylor 2000; El Mouden et al. A total of 12 agamid species representing 8 genera were 2001;UllerandOlsson2006; Uller et al. 2006). collected from various locations around Australia Australian agamids (ca. 70 species; Cogger 2000) (Table 1). Six of these species have GSD, three have represent a recent radiation (∼25 Mya) from an TSD, and in the remaining three species the sex- Asian ancestor (Hugall et al. 2008), and show a determining mechanism is uncertain. One male and distribution of GSD and TSD mechanisms suggest- one female were examined from each of the species ing an evolutionary history involving multiple except for Diporiphora bilineata and Tympanocryptis independent origins of one, and possibly both, of pinguicolla (one male only) and Chlamydosaurus these mechanisms of sex determination. Both GSD kingii (one female only). and TSD species can occur within the same genus Animals were euthanized by intraperitoneal injec- (Harlow 2000, 2004; Harlow and Taylor 2000;Uller tion of sodium pentobarbitone at a concentration of and Olsson 2006, Uller et al. 2006), and in at least 150 μg/g body weight. Phenotypic sex was deter- one species, the central bearded dragon (Pogona mined on the basis of external morphology, hemipene vitticeps), there is an interaction between genotype eversion (Harlow 1996), and by internal examination and egg incubation temperature in sex determination of gonadal morphology. Fibroblastic cultures were (Quinn et al. 2007). established from macerated explants of eye, pericar- Karyotypes are highly conserved among Australian dium or tail tip tissue. For larger animals, 0.2–1ml
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