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Conservation of Sex Chromosomes in Lacertid Lizards

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Conservation of Sex Chromosomes in Lacertid Lizards Molecular Ecology (2016) doi: 10.1111/mec.13635 Conservation of sex chromosomes in lacertid lizards MICHAIL ROVATSOS,* JASNA VUKIC,* MARIE ALTMANOVA,* MARTINA JOHNSON POKORNA,*† JIRI MORAVEC‡ and LUKASKRATOCHVIL* *Department of Ecology, Faculty of Science, Charles University in Prague, Vinicna 7, 128 44 Prague, Czech Republic, †Institute of Animal Physiology and Genetics, The Czech Academy of Sciences, Libechov, Czech Republic, ‡Department of Zoology, National Museum, Vaclavskenam. 68, 115 79 Prague, Czech Republic Abstract Sex chromosomes are believed to be stable in endotherms, but young and evolutionary unstable in most ectothermic vertebrates. Within lacertids, the widely radiated lizard group, sex chromosomes have been reported to vary in morphology and heterochroma- tinization, which may suggest turnovers during the evolution of the group. We compared the partial gene content of the Z-specific part of sex chromosomes across major lineages of lacertids and discovered a strong evolutionary stability of sex chromosomes. We can conclude that the common ancestor of lacertids, living around 70 million years ago (Mya), already had the same highly differentiated sex chromosomes. Molecular data demonstrating an evolutionary conservation of sex chro- mosomes have also been documented for iguanas and caenophidian snakes. It seems that differences in the evolutionary conservation of sex chromosomes in vertebrates do not reflect the distinction between endotherms and ectotherms, but rather between amniotes and anamniotes, or generally, the differences in the life history of particular lineages. Keywords: lizards, molecular sexing, reptiles, sex chromosomes Received 29 December 2015; revision received 7 March 2016; accepted 22 March 2016 Organ & Janes 2008; Grossen et al. 2011), and as a whole, Introduction they indeed exhibit a large variability in sex-determining In vertebrates, the gonad is not differentiated early in systems. However, this variability seems to be dis- ontogeny and only later develops into testicular or ovar- tributed unequally among particular reptile lineages. As ian structures. Although the genetic framework for the far as is known, all crocodiles share environmental sex differentiation of testes or ovaries is highly conserved, determination (ESD; Valenzuela & Lance 2004), where the process of sex determination which decides whether the sex of an individual is decided by environmental the undifferentiated gonad will turn into a testis or an conditions during the sensitive period of embryonic ovary, is surprisingly variable. Also, the rate of turn- development. In comparison, turtles and lepidosaurs (tu- overs of sex-determining mechanisms is notably differ- ataras and squamates) possess variability in sex-deter- ent among particular vertebrate lineages. Some mining systems, and both ESD and genotypic sex ectothermic lineages, such as several well-studied determination (GSD, where the sex of an individual is groups of fish or frogs, possess a rapid turnover of sex set by its sex-specific genotype) can be found in different chromosomes (Miura 2007; Kikuchi & Hamaguchi 2013; species of these lineages (Janzen & Phillips 2006; Dufresnes et al. 2015), while endotherms, that is mam- Pokorna & Kratochvıl 2009; Valenzuela & Adams 2011; mals and birds, have highly conserved sex chromosomes Gamble et al. 2015; Johnson Pokorna & Kratochvıl 2016). (e.g. Shetty et al. 1999; Graves 2006). As ectotherms, rep- Nevertheless, based on the phylogenetic distribution of tiles are usually considered as a group with a rapid turn- the types of sex chromosomes given by classical cytoge- over of sex-determining mechanisms (Sarre et al. 2004; netic data (Pokorna & Kratochvıl 2009; Gamble et al. 2015), some lineages of squamates might possess evolu- Correspondence: Lukas Kratochvıl, Fax: +420 221951673; tionary highly conserved sex chromosomes, although the E-mail: [email protected] cytogenetic data might not always be reliable in © 2016 John Wiley & Sons Ltd 2 M. ROVATSOS ET AL. demonstrating the homology of sex chromosomes. Cyto- neo-sex chromosomes (Rojo et al. 2014; reviewed in genetically similar sex chromosomes might appear to be Pokorna et al. 2014a), the Z and W sex chromosomes nonhomologous in related lineages (Vicoso & Bachtrog are believed to be rather homomorphic and are only 2015), and on the other hand, sex chromosomes can be cytogenetically distinguishable by C-banding detection homologous in spite of observed variability in morphol- of the notable heterochromatin accumulation on the W ogy and heterochromatinization (Rovatsos et al. 2014a,b; chromosomes (Olmo et al. 1987; Pokorna et al. 2011a). Altmanova et al. 2016). Despite significant progress in The heterochromatization of the W chromosome is recent years, molecular data on the evolutionary stability likely a result of its considerable degeneration. In some of sex chromosomes among squamates exist only for species, the W chromosome contains an enormous accu- iguanas (Pleurodonta; Rovatsos et al. 2014a,b) and caeno- mulation of repetitive elements (Pokorna et al. 2011a in phidian snakes (e.g. Matsubara et al. 2006; Vicoso et al. Eremias velox), while sex chromosome size differs across 2013; Rovatsos et al. 2015). These studies show that at lacertid species and W chromosomes are euchromatic in least in some cases, conservation of sex chromosomes in certain lacertid lineages (Olmo et al. 1987). The latter ectothermic vertebrates can be comparable to fact led to the hypothesis that differentiation of sex endotherms, but little is known whether snakes and chromosomes took place repeatedly and independently iguanas are rules or exceptions to the more general pat- in different taxa within the family (Odierna et al. 1993). tern. Alternatively, nonhomologous sex chromosomes may The lizards of the family Lacertidae represent a very be present in different lineages in lacertids. The gene important part of diurnally active reptiles in Europe, content of the Z chromosome was reported in the Asia, Africa and adjacent islands (for instance, they Swedish population of Lacerta agilis (Srikulnath et al. play a very important ecological role in many Mediter- 2014), where the lacertid Z chromosome was suggested ranean islands and in the Canary Islands). They occupy to be homologous to a part of the third largest chromo- an extensive range of environments, from rain forests some pair of Anolis carolinensis, the model species for through to deserts, with the notable case of the lizard reptile genomics. However, the analysis of transcrip- Zootoca vivipara, having a wide distribution across the tome in Takydromus sexlinaeatus and the test of Z-specifi- Palearctic region, from Europe to Japan and even north city based on qPCR in this species and in the Czech of the Polar Circle. Lacertids are mostly terrestrial, but population of Lacerta agilis revealed that the genes from several species are saxicolous or even arboreal and this region are in fact not Z-specific (Rovatsos et al. partly fossorial (Pough et al. 2003). Currently, 322 spe- 2016). This finding suggests either a turnover of sex cies categorized into 42 genera have been recognized chromosomes within Lacerta agilis, several turnovers of (Uetz & Hosek 2015). The phylogenetic relationships sex chromosomes in lacertids as a whole or the among lacertids are not fully resolved, and conflicting misidentification of the Z-specific region in the previous topologies can be found among recent phylogenetic study (Srikulnath et al. 2014). Only, further comparative studies based on molecular data (Arnold et al. 2007; study within lacertids can resolve this issue and Mayer & Pavlicev 2007; Pyron et al. 2013). However, the uncover the degree of conservation of sex chromosomes splitting of the family into two subfamilies (Gallotiinae in this clade. In this study, we tested the competing and Lacertinae with two tribes: Eremiadini and Lacer- hypotheses on homology and differentiation of sex tini) has been well supported and now accepted. The chromosomes across lacertids. precise age of the group is not known, but the split between lacertids and their likely sister group, limbless Materials and methods fossorial amphisbaenians, has been estimated at approx- imately 110–130 Mya (Hedges et al. 2006), while the Material and ethics statement basal divergence just within the tribe Lacertini based on molecular clocks was estimated to be the surprisingly Tissue or blood samples in ethanol were acquired from young age of 12–16 Mya (Arnold et al. 2007). 32 individuals from 16 species of lacertids (one male Studies have revealed that lacertids possess GSD and one female per species), covering all major lacertid (reviewed, e.g. in Pokorna & Kratochvıl 2009, one older clades (Table S1, Supporting information). Particular report of ESD in a single species, Podarcis pityusensis,is attention was taken to include as many species from the dubious; see, e.g. critical review in Pokorna& genus Lacerta and its close relatives (genera Timon and Kratochvıl 2009). Obligatory unisexuality exists within Podarcis) as possible, as previous studies have suggested the genus Darevskia (e.g. Kupriyanova 2010). Wherever a variation in sex chromosomes within this genus known, sex chromosomes of lacertids point to a female (Srikulnath et al. 2014; cf. to Rovatsos et al. 2016). heterogamety (reviewed in Olmo & Signorino 2015). All experimental procedures were carried out under With the exception of several lineages with multiple the supervision and with the approval of the
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