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Cross-Species BAC Mapping Highlights Conservation of Chromosome Synteny Across Dragon Lizards (Squamata: Agamidae)

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Cross-Species BAC Mapping Highlights Conservation of Chromosome Synteny Across Dragon Lizards (Squamata: Agamidae) G C A T T A C G G C A T genes Article Cross-Species BAC Mapping Highlights Conservation of Chromosome Synteny across Dragon Lizards (Squamata: Agamidae) Shayer Mahmood Ibney Alam 1,* , Marie Altmanová 2 , Tulyawat Prasongmaneerut 3 , Arthur Georges 1 , Stephen D. Sarre 1 , Stuart V. Nielsen 4,5, Tony Gamble 4,6,7, Kornsorn Srikulnath 3 , Michail Rovatsos 2 , Lukáš Kratochvíl 2 and Tariq Ezaz 1,* 1 Institute for Applied Ecology, University of Canberra, Bruce, ACT 2617, Australia; [email protected] (A.G.); [email protected] (S.D.S.) 2 Department of Ecology, Faculty of Science, Charles University, 12844 Prague, Czech Republic; [email protected] (M.A.); [email protected] (M.R.); [email protected] (L.K.) 3 Laboratory of Animal Cytogenetics & Comparative Genomics, Department of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand; [email protected] (T.P.); [email protected] (K.S.) 4 Department of Biological Sciences, Marquette University, Milwaukee, WI 53233, USA; [email protected] (S.V.N.); [email protected] (T.G.) 5 Division of Herpetology, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA 6 Milwaukee Public Museum, 800 W. Wells St., Milwaukee, WI 53233, USA 7 Bell Museum of Natural History, University of Minnesota, 2088 Larpenteur Ave. W., St. Paul, MN 55113, USA * Correspondence: [email protected] (S.M.I.A.); [email protected] (T.E.) Received: 18 May 2020; Accepted: 22 June 2020; Published: 25 June 2020 Abstract: Dragon lizards (Squamata: Agamidae) comprise about 520 species in six subfamilies distributed across Asia, Australasia and Africa. Only five species are known to have sex chromosomes. All of them possess ZZ/ZW sex chromosomes, which are microchromosomes in four species from the subfamily Amphibolurinae, but much larger in Phrynocephalus vlangalii from the subfamily Agaminae. In most previous studies of these sex chromosomes, the focus has been on Australian species from the subfamily Amphibolurinae, but only the sex chromosomes of the Australian central bearded dragon (Pogona vitticeps) are well-characterized cytogenetically. To determine the level of synteny of the sex chromosomes of P. vitticeps across agamid subfamilies, we performed cross-species two-colour FISH using two bacterial artificial chromosome (BAC) clones from the pseudo-autosomal regions of P. vitticeps. We mapped these two BACs across representative species from all six subfamilies as well as two species of chameleons, the sister group to agamids. We found that one of these BAC sequences is conserved in macrochromosomes and the other in microchromosomes across the agamid lineages. However, within the Amphibolurinae, there is evidence of multiple chromosomal rearrangements with one of the BACs mapping to the second-largest chromosome pair and to the microchromosomes in multiple species including the sex chromosomes of P. vitticeps. Intriguingly, no hybridization signal was observed in chameleons for either of these BACs, suggesting a likely agamid origin of these sequences. Our study shows lineage-specific evolution of sequences/syntenic blocks and successive rearrangements and reveals a complex history of sequences leading to their association with important biological processes such as the evolution of sex chromosomes and sex determination. Keywords: agamid lizards; sex chromosomes; BACs; synteny; evolution; FISH Genes 2020, 11, 698; doi:10.3390/genes11060698 www.mdpi.com/journal/genes Genes 2020, 11, 698 2 of 12 1. Introduction Reptiles are well known for their diverse modes of sex determination and sex chromosomes [1,2]. They exhibit large variability in the degree of differentiation of sex chromosomes ranging from homomorphic to heteromorphic in structure [2–5]. Squamate reptiles (lizards, snakes and amphisbaenians) are the most diverse reptile group in terms of species diversity and mode of sex determination [1,6]. The variability seen among squamateGenes sex 2020 chromosomes, 11, x FOR PEER REVIEW suggests that sex chromosome and sex determination2 of 13 systems have evolved independently1. Introduction many times. Non-homologous sex chromosomes have been reported even among relatively closely relatedReptiles species are well [ 2known,5,7]. for The their same diverse parts modes of of the sex genome determination (i.e., and homologous sex chromosomes regions) have been found to play the[1,2 role]. They of exhibit sex chromosomes large variability in inthe differentdegree of differentiation vertebrate of taxasex chromosomes [5,8–11]. Aranging high from degree of synteny homomorphic to heteromorphic in structure [2–5]. Squamate reptiles (lizards, snakes and has been observedamphisbaenians) between birdsare the andmost squamatediverse reptile reptiles group in owingterms of species to a relative diversity lowand mode degree of sex of chromosomal rearrangementsdetermination in this group [1,6] [.5 The,12 –variability18]. Temperature-dependent seen among squamate sex chromosomes sex determination suggests that (TSD), sex genotypic sex chromosome and sex determination systems have evolved independently many times. Non- determination (GSD),homologous and sex GSD chromosomes with temperature have been reported influences even among between relatively relativelyclosely related closely species related species make squamate[ lizards2,5,7]. The an same interesting parts of the genome group (i.e. to, studyhomologous and regions) understand have been the found evolution to play the ofrole sex of chromosomes. Agamid lizardssex chromosomes (Squamata: in different Agamidae), vertebrate commonlytaxa [5,8–11]. A known high degree as of dragons synteny has in been Australasia, observed are notorious between birds and squamate reptiles owing to a relative low degree of chromosomal rearrangements for their variabilityin this in formsgroup of[5,12 sex–18] determination. Temperature-dependent [19–23 s].ex Together determination with (TSD), chameleons genotypic (Chamaeleonidae),sex they form the iguaniandetermination clade (GSD), Acrodonta, and GSD with sistertemperature to iguanas influences (Pleurodonta)between relatively [closely24,25 ].related Acrodonts are an species make squamate lizards an interesting group to study and understand the evolution of sex interesting groupchromosomes. in terms of the evolution and diversity of sex determination [7,26,27], while the iguanas have, withA onegamid exception lizards (Squamata: (basilisks), Agamidae) conserved, commonly XXknown/XY as sexdragons chromosomes in Australasia, [are28 ,29]. There are notorious for their variability in forms of sex determination [19–23]. Together with chameleons about 520 currently(Chamaeleonidae), described they agamid form the iguanian species clade [6] Acrodonta, comprising sister to six iguanas subfamilies (Pleurodonta) that [24,25 diverged]. around 70–120 millionAcrodonts years ago are an [25 interesting,30]. Most group agamid in terms of species the evolution are and oviparous diversity of [ 6sex], anddetermination the groups includes species with obligate[7,26,27], andwhile facultativethe iguanas have parthenogenesis, with one exception (basilisks) [31–33, conserv]. Sexed determination XX/XY sex chromosome modes is relatively [28,29]. There are about 520 currently described agamid species [6] comprising six subfamilies that well studied indiverged a few around species 70–120 from million the years subfamily ago [25,30]. AmphibolurinaeMost agamid species are [ 7oviparous,19], but [6], notand the in the other five subfamilies (Figuregroups1 ),includes highlighting species with a obligate significant and facultative gap in parthenogenesis our understanding [31–33]. Sex of determination how sex chromosomes mode is relatively well studied in a few species from the subfamily Amphibolurinae [7,19], but not evolved in thisin widespread the other five subfamilies and chromosomally (Figure 1), highlighting variable a significant family. gap in our understanding of how sex chromosomes evolved in this widespread and chromosomally variable family. Uromastycinae Draconinae Agaminae Leiolepidinae Hydrosaurinae Amphibolurinae ZZ/ZW TSD Figure 1. EstimatedFigure 1. distribution Estimated distribution of the ofagamid the agamid subfamilies subfamilies together together with known with sex known determination sex determination mechanisms [6,mechanisms17,20,21, 24[6,17,20,21,24,31,34,31,34–49].– The49]. The species species of the the subfamily subfamily Draconinae Draconinae are distributed are over distributed over South and Southeast Asia, Agaminae across Africa and Asia, Amphibolurinae across Australia, Papua South and Southeast Asia, Agaminae across Africa and Asia, Amphibolurinae across Australia, Papua New Guinea and Southeast Asia, Hydrosaurinae across Papua New Guinea, the Philippines and Indonesia, Leiolepidinae across Southeast Asia and Uromastycinae across Africa and South Asia. TSD—temperature dependent sex determination, ZZ/ZW—female heterogamety. Obligatory parthenogenesis has been reported in several species of the subfamily Leiolepidinae, although the sex determination system is not known in this lineage. Genes 2020, 11, 698 3 of 12 Only about one fifth (91 species) of Agamid species have been karyotyped, with diploid chromosome numbers ranging from 2n = 32 to 2n = 54 [4,6,50]. Agamids exhibit a diverse array of sex-determination mechanisms that include TSD, GSD and GSD with sex reversal [1,2,22,39,51]. Sex chromosomes have only been identified
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