Iguanians (Pleurodonta) are one of the reptile lineages that, like birds and mammals, have sex chromosomes of ancient origin. In most iguanians these are microchromosomes, making a distinction between the X and Y as well as between homeologous sex chromosomes in other species difficult. Meiotic chromosome analysis may be used to elucidate their differentiation, because meiotic prophase chromosomes are longer and less condensed than metaphase chromosomes, and the homologues are paired with each other, revealing minor heteromorphisms. Using electron and fluorescent microscopy of surface spread synaptonemal complexes (SCs) and immunolocalization of the proteins of the SC (SYCP3), the centromere, and recombination nodules (MLH1), we examined sex chromosome synapsis and recombination in 2 species of anoles (Dactyloidae), Anolis carolinensis and Deiroptyx coelestinus, in which the sex chromosomes represent the ancestral condition of iguanians. We detected clear differences in size between the anole X and Y microchromosomes and found an interspecies difference in the localization of the pseudoautosomal region. Our results show that the apparent homomorphy of certain reptile sex chromosome systems can hide a cryptic differentiation, which potentially may influence the evolution of sexual dimorphism and speciation.

1.
Alföldi J, Di Palma F, Grabherr M, Williams C, Kong L, et al: The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477:587-591 (2011).
2.
Altmanová M, Rovatsos M, Kratochvíl L, Johnson Pokorná M: Minute Y chromosomes and karyotype evolution in Madagascan iguanas (Squamata: Iguania: Opluridae). Biol J Linn Soc 18:618-633 (2016).
3.
Anderson LK, Reeves A, Webb LM, Ashley T: Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151:1569-1579 (1999).
4.
Carrasco LA, Penman DJ, Bromage N: Evidence for the presence of sex chromosomes in the Nile tilapia (Oreochromis niloticus) from synaptonemal complex analysis of XX, XY and YY genotypes. Aquaculture 173:207-218 (1999).
5.
Castiglia R, Flores-Villela O, Bezerra AMR, Muñoz A, Gornung E: Pattern of chromosomal changes in “beta” Anolis (Norops group) (Squamata: Polychrotidae) depicted by an ancestral state analysis. Zool Studies 52:60 (2013).
6.
Charlesworth B, Sniegowski P, Stephan W: The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215-220 (1994).
7.
Deakin JE, Edwards MJ, Patel H, O'Meally D, Lian J, et al: Anchoring genome sequence to chromosomes of the central bearded dragon (Pogona vitticeps) enables reconstruction of ancestral squamate macrochromosomes and identifies sequence content of the Z chromosome. BMC Genomics 17:447 (2016).
8.
Ezaz T, Sarre SD, O'Meally D, Graves JA, Georges A: Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res 127:249-260 (2009).
9.
Gamble T, Geneva AJ, Glor RE, Zarkower D: Anolis sex chromosomes are derived from a single ancestral pair. Evolution 68:1027-1041 (2014).
10.
Giovannotti M, Trifonov VA, Paoletti A, Kichigin IG, O'Brien PCM, et al: New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae). Chromosoma, Epub ahead of print (2016).
11.
Gorman GC: The chromosomes of the reptilian: a cytotaxonomic interpretation, in Chiarelli B, Capanna E (eds): Cytotaxonomy and Vertebrate Evolution, pp 349-424 (Academic Press, London 1973).
12.
Graves JAM: Sex chromosome specialization and degeneration in mammals. Cell 124:901-914 (2006).
13.
Graves JAM: Did sex chromosome turnover promote divergence of the major mammal groups? De novo sex chromosomes and drastic rearrangements may have posed reproductive barriers between monotremes, marsupials and placental mammals. Bioessays 38:734-743 (2016).
14.
Howell WT, Black DA: Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36:1014-1015 (1980).
15.
Kichigin IG, Giovannotti M, Makunin AI, Ng BL, Kabilov MR, et al: Evolutionary dynamics of Anolis sex chromosomes revealed by sequencing of flow sorting-derived microchromosome-specific DNA. Mol Genet Genomics 291:1955-1966 (2016).
16.
Lisachov AP, Borodin PM: Microchromosome polymorphism in the sand lizard, Lacerta agilis Linnaeus, 1758 (Reptilia, Squamata). Comp Cytogenet 10:387-399 (2016).
17.
Lisachov AP, Zadesenets KS, Rubtsov NB, Borodin PM: Sex chromosome synapsis and recombination in male guppies. Zebrafish 12:174-180 (2015).
18.
Mank JE, Ellegren H: Parallel divergence and degradation of the avian W sex chromosome. Trends Ecol Evol 22:389-391 (2007).
19.
Nicholson KE, Crother BI, Guyer C, Savage JM: It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa 3477:1-108 (2012).
20.
Olmo E, Signorino G: Chromorep: A Reptiles Chromosomes Database (2005). http://chromorep.univpm.it (accessed November 7, 2016).
21.
Peters AH, Plug AW, van Vugt MJ, de Boer P: A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5:66-68 (1997).
22.
Pigozzi MI: Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Genome Res 95:129-133 (2001).
23.
Pigozzi MI: Diverse stages of sex-chromosome differentiation in tinamid birds: evidence from crossover analysis in Eudromia elegans and Crypturellus tataupa. Genetica 139:771-777 (2011).
24.
Pigozzi MI, Solari AJ: Meiotic recombination in the ZW pair of a tinamid bird shows a differential pattern compared with neognaths. Genome 48:286-290 (2005).
25.
Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, et al: Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94 (2007).
26.
Pyron RA, Burbrink FT, Wiens JJ: A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:93 (2013).
27.
Reed KM, Sudman PD, Sites JW Jr, Greenbaum IF: Synaptonemal complex analysis of sex chromosomes in two species of Sceloporus. Copeia 1990:1122-1129 (1990).
28.
Reeves A: MicroMeasure: a new computer program for the collection and analysis of cytogenetic data. Genome 44:439-443 (2001).
29.
Rovatsos M, Altmanová M, Pokorná M, Kratochvíl L: Conserved sex chromosomes across adaptively radiated Anolis lizards. Evolution 68:2079-2085 (2014a).
30.
Rovatsos M, Altmanová M, Pokorná MJ, Kratochvíl L: Novel X-linked genes revealed by quantitative polymerase chain reaction in the green anole, Anolis carolinensis. G3 (Bethesda) 4:2107-2113 (2014b).
31.
Rovatsos M, Vukić J, Lymberakis P, Kratochvíl L: Evolutionary stability of sex chromosomes in snakes. Proc Biol Sci 282:20151992 (2015).
32.
Solari AJ: Equalization of Z and W axes in chicken and quail oocytes. Cytogenet Genome Res 59:52-56 (1992).
33.
Srikulnath K, Matsubara K, Uno Y, Nishida C, Olsson M, Matsuda Y: Identification of the linkage group of the Z sex chromosomes of the sand lizard (Lacerta agilis, Lacertidae) and elucidation of karyotype evolution in lacertid lizards. Chromosoma 123:563-575 (2014).
34.
Srikulnath K, Uno Y, Nishida C, Ota H, Matsuda Y: Karyotype reorganization in the Hokou gecko (Gekko hokouensis, Gekkonidae): the process of microchromosome disappearance in Gekkota. PLoS One 10:e0134829 (2015).
35.
Traut W, Winking H: Meiotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platyfish and guppy. Chromosome Res 9:659-672 (2001).
36.
Uetz P, Freed P, Hošek J: The Reptile Database, http://www.reptile-database.org (accessed November 10, 2016).
37.
Veyrunes F, Waters PD, Miethke P, Rens W, McMillan D, et al: Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res 18:965-973 (2008).
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