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Conserved ZZ/ZW Sex Chromosomes in Caribbean Croaking Geckos (Aristelliger: Sphaerodactylidae)

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Conserved ZZ/ZW Sex Chromosomes in Caribbean Croaking Geckos (Aristelliger: Sphaerodactylidae) Received: 12 February 2020 | Revised: 22 June 2020 | Accepted: 2 July 2020 DOI: 10.1111/jeb.13682 RESEARCH PAPER Conserved ZZ/ZW sex chromosomes in Caribbean croaking geckos (Aristelliger: Sphaerodactylidae) Shannon E. Keating1 | Aaron H. Griffing1 | Stuart V. Nielsen1,2 | Daniel P. Scantlebury3 | Tony Gamble1,4,5 1Department of Biological Sciences, Marquette University, Milwaukee, WI, USA Abstract 2Florida Museum of Natural History, Current understanding of sex chromosome evolution is largely dependent on spe- University of Florida, Gainesville, FL, USA cies with highly degenerated, heteromorphic sex chromosomes, but by studying spe- 3Resonate, Reston, VA, USA cies with recently evolved or morphologically indistinct sex chromosomes we can 4Milwaukee Public Museum, Milwaukee, WI, USA greatly increase our understanding of sex chromosome origins, degeneration and 5Bell Museum of Natural History, University turnover. Here, we examine sex chromosome evolution and stability in the gecko of Minnesota, Saint Paul, MN, USA genus Aristelliger. We used RADseq to identify sex-specific markers and show that Correspondence four Aristelliger species, spanning the phylogenetic breadth of the genus, share a Shannon E. Keating, Department of conserved ZZ/ZW system syntenic with avian chromosome 2. These conserved sex Biological Sciences, Marquette University, Wehr Life Sciences, 109 1428 W. Clybourn chromosomes contrast with many other gecko sex chromosome systems by showing Street, Milwaukee, WI 53233, USA. a degree of stability among a group known for its dynamic sex-determining mecha- Email: [email protected] nisms. Cytogenetic data from A. expectatus revealed homomorphic sex chromosomes Funding information with an accumulation of repetitive elements on the W chromosome. Taken together, National Science Foundation, Grant/Award Number: DEB-0920892, DEB-1110605 and the large number of female-specific A. praesignis RAD markers and the accumula- IOS1146820 tion of repetitive DNA on the A. expectatus W karyotype suggest that the Z and W chromosomes are highly differentiated despite their overall morphological similarity. We discuss this paradoxical situation and suggest that it may, in fact, be common in many animal species. KEYWORDS cytogenetics, Gekkota, lizard, RADseq, reptile, sex chromosomes 1 | INTRODUCTION (the X/Y and Z/W) prevents DNA repair and can lead to an accumu- lation of deleterious mutations and repetitive DNAs on the sex-spe- Sex chromosomes evolve from an autosomal chromosome pair that cific chromosome (the Y or W; Charlesworth, 1991; Charlesworth acquires a sex-determining locus. The canonical model of sex chro- & Charlesworth, 2000). Given sufficient time, this degeneration mosome evolution suggests linkage between the sex-determining can result in a pair of morphologically distinct, or heteromorphic, locus and some neighbouring sexually antagonistic allele occurs via sex chromosomes. Historically, cytogenetic methods were used to recombination suppression between the X and Y (or Z and W) chro- identify a species’ sex chromosome system based on the presence of mosomes (Charlesworth, 1991; Muller, 1914; Ohno, 1967). However, these heteromorphic sex chromosomes in one sex and not the other. recombination suppression between the proto-sex chromosomes However, when taxa exhibit morphologically similar (homomorphic) Data deposited at Dryad: https://doi.org/10.5061/dryad.573n5 tb51 The peer review history for this article is available at https://publo ns.com/publo n/10.1111/jeb.13682. © 2020 European Society For Evolutionary Biology. Journal of Evolutionary Biology © 2020 European Society For Evolutionary Biology 1316 | wileyonlinelibrary.com/journal/jeb J Evol Biol. 2020;33:1316–1326. KEATING et AL. | 1317 sex chromosomes, classic cytogenetic methods fall short. This has RADseq methods have been used to successfully identify additional led to large knowledge gaps concerning the taxonomic distribution of XX/XY species (Sphaerodactylus nicholsi, S. inigoi and Gonatodes sex chromosomes (Bachtrog et al., 2014; Devlin & Nagahama, 2002; ferrugineus) as well as the first (and currently only) sphaerodactylid Ezaz, Sarre, O’Meally, Graves, & Georges, 2009; Gamble & species with a ZZ/ZW sex chromosome system, Aristelliger expecta- Zarkower, 2014; Matsubara et al., 2006; Schmid & Steinlein, 2001; tus (Gamble et al., 2015, 2018). This suggests a minimum of one sex Stöck et al., 2011). chromosome transition in the Sphaerodactylidae. Based on the high The advent of high-throughput DNA sequencing has led to new level of sex chromosome turnover observed in other gecko clades, methods for identifying homomorphic sex chromosomes, resulting additional transitions are likely to be uncovered as more data are in a rapid expansion of our knowledge of sex chromosome systems generated. across the tree of life (Gamble, 2016). One such method uses genetic The sphaerodactylid genus Aristelliger, commonly known as croak- markers generated via restriction site-associated DNA sequencing ing geckos, is comprised of nine species distributed in the Caribbean (RADseq; Baird et al., 2008), which utilizes the naturally occurring and Central America (Bauer & Russell, 1993; Diaz & Hedges, 2009; restriction enzyme cut sites distributed throughout the genome Schwartz & Henderson, 1991). This charismatic group diverged to generate tens of thousands of markers (RADtags). Comparing from its sister genus Quedenfeldtia approximately 70 million years RADtags from multiple males and females of a species can identify ago (Gamble, Bauer, et al., 2011) and differs from other New World a small fraction of markers that corresponds to the sex-specific sex sphaerodactylids in being nocturnal, arboreal, possessing large basal chromosomes (i.e. the Y or the W). Species with an abundance of adhesive toepads, and exhibiting the largest range of body sizes of all male-specific RAD markers have an XX/XY sex chromosome system, sphaerodactylids (Griffing, Daza, DeBoer, & Bauer, 2018; Henderson and species with an abundance of female-specific RAD markers have & Powell, 2009; Schwartz & Henderson, 1991). As previously men- a ZZ/ZW system (Gamble et al., 2015; Gamble & Zarkower, 2014; tioned, Aristelliger expectatus represents the only sphaerodactylid Pan et al., 2016). This method has been used to identify homo- species with a confirmed ZZ/ZW sex chromosome system (Gamble morphic sex chromosomes across a wide range of taxa (Fowler & et al., 2015). Here, we combine newly generated RADseq data with Buonaccorsi, 2016; Gamble et al., 2015; Jeffries et al., 2018; Nielsen, traditional cytogenetics to identify and characterize sex chromo- Daza, Pinto, & Gamble, 2019; Pan et al., 2016) and detect import- somes in three additional Aristelliger species, A. praesignis, A. lar and ant and unexpected transitions among sex chromosomes (Gamble A. barbouri. We focus on two main questions: (1) Do other species of et al., 2017; Nielsen, Banks, Diaz, Trainor, & Gamble, 2018). Such Aristelliger possess a ZZ/ZW sex chromosome system? And, if so, (2) methods, particularly when combined with modern cytogenetics are the sex chromosomes homologous across the genus? In contrast (Deakin et al., 2019), are building a greater foundation on which to with what has been observed in other geckos, a group noted for dy- study the evolutionary processes governing sex chromosome ori- namic sex chromosome turnover, we here recover a conserved sex gins, degeneration and stability. chromosome system among all sampled Aristelliger species. Gecko lizards exhibit both male and female heterogamety as well as temperature-dependent sex determination (TSD), wherein egg incubation temperature determines sex. Notably, geckos ex- 2 | MATERIALS AND METHODS hibit the highest number of identified sex-determining system tran- sitions of any amniote group with between 17 and 25 transitions 2.1 | RADseq identified thus far (Gamble, 2010; Gamble et al., 2015). The gecko family Sphaerodactylidae consists of over 200 species in 12 gen- We extracted DNA from eleven males and ten females of A. prae- era broadly distributed in South America, the Caribbean, North signis using the QIAGEN DNeasy Blood and Tissue Kit (Table S2). We Africa, the Middle East and Central Asia (Gamble, Bauer, et al., 2011; generated single-digest RADseq libraries using a modified protocol Gamble, Bauer, Greenbaum, & Jackman, 2008; Gamble, Daza, Colli, from Etter, Bassham, Hohenlohe, Johnson, and Cresko (2012) as de- Vitt, & Bauer, 2011). Despite this rich species diversity, sex-deter- scribed in Gamble et al. (2015). Briefly, we digested genomic DNA mining systems are known in only a handful of species. Of the 12 using a high-fidelity Sbf1 restriction enzyme (New England Biolabs) sphaerodactylid species that have been karyotyped (Table S1), only and ligated individually barcoded P1 adapters to each sample. We one, the XX/XY species Eupletes europaea, can confidently be said to pooled samples into multiple libraries, sonicated and size-selected possess heteromorphic sex chromosomes (Gamble, 2010; Gornung, for 200- to 500-bp fragments using magnetic beads in a PEG/ Mosconi, Annesi, & Castiglia, 2013). Gonatodes ceciliae has heter- NaCl buffer (Rohland & Reich, 2012). We then blunt-end-repaired, omorphic chromosomes, which have been interpreted as XX/XY dA-tailed and ligated pooled libraries with a P2 adapter contain- sex chromosomes (McBee, Bickham, & Dixon., 1987). However, the ing unique Illumina barcodes. Pooled libraries were amplified using diverse karyotypes among
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