Pleurodont lizards are characterized by an ancient system of sex chromosomes. Along with stability of the central component of the system (homologous to the X chromosome of Anolis carolinensis [Dactyloidae], ACAX), in some genera the ancestral sex chromosomes are fused with microautosomes, forming neo-sex chromosomes. The genus Ctenonotus (Dactyloidae) is characterized by multiple X1X1X2X2/X1X2Y sex chromosomes. According to cytogenetic data, the large neo-Y chromosome is formed by fusion of the ancestral Y chromosome with 2 microautosomes (homologous to ACA10 or ACA11 and ACA12), the X1 chromosome is formed by fusion of the ancestral X chromosome with the autosome homologous to ACA10 or ACA11, and the X2 chromosome is homologous to autosome ACA12. To determine more precisely the content and evolution of the Ctenonotus sex chromosomes, we sequenced flow-sorted chromosomes (both sex chromosomes and microautosomes as control) of 2 species with a similar system: C. pogus and C. sabanus. Our results indicate that the translocated part of the X1 is homologous to ACA11, X2 is homologous to ACA12, and the Y contains segments homologous to both ACA11 and ACA12. Molecular divergence estimates suggest that the ancestral X-derived part has completely degenerated in the Y of Ctenonotus, similar to the degeneration of the Norops sagrei Y chromosome (Dactyloidae). The newly added regions show loss of DNA content, but without degeneration of the conserved regions. We hypothesize that the translocation of autosomal blocks onto sex chromosomes facilitated rapid degeneration of the pseudoautosomal region on the ancestral Y.

Keywords:
Gonosome evolution, Lizards, Next-generation sequencing, Reptile, Sex chromosomes, Degeneration
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.
Bachtrog D: Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14:113-124 (2013).
3.
Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, et al: Sex determination: why so many ways of doing it? PLoS Biol 12:e1001899 (2014).
4.
Borodin PM, Basheva EA, Dashkevich OA, Golenishchev FN, Kartavtseva IV: X-Y chromosome synapsis and recombination in 3 vole species of Asian lineage of the genus Microtus (Rodentia: Arvicolinae). Cytogenet Genome Res 132:129-133 (2011).
5.
Brinkrolf K, Rupp O, Laux H, Kollin F, Ernst W, et al: Chinese hamster genome sequenced from sorted chromosomes. Nat Biotechnol 31:694-695 (2013).
6.
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).
7.
Fleishman LJ, Pallus AC: Motion perception and visual signal design in Anolis lizards. Proc Biol Sci 277:3547-3554 (2010).
8.
Gamble T, Geneva AJ, Glor RE, Zarkower D: Anolis sex chromosomes are derived from a single ancestral pair. Evolution 68:1027-1041 (2014).
9.
Gamble T, Coryell J, Ezaz T, Lynch J, Scantlebury DP, Zarkower D: Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol Biol Evol 32:1296-1309 (2015).
10.
Gamble T, Castoe TA, Nielsen SV, Banks JL, Card DC, et al: The discovery of XY sex chromosomes in a Boa and Python. Curr Biol 27:2148-2153 (2017).
11.
Giovannotti M, Caputo V, O'Brien PCM, Lovell FL, Trifonov V, et al: Skinks (Reptilia: Scincidae) have highly conserved karyotypes as revealed by chromosome painting. Cytogenet Genome Res 127:224-231 (2009).
12.
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 126:245-260 (2017).
13.
Hertz PE, Arima Y, Harrison A, Huey RB, Losos JB, Glor RE: Asynchronous evolution of physiology and morphology in Anolis lizards. Evolution 67:2101-2113 (2013).
14.
Holleley CE, O'Meally D, Sarre SD, Graves JAM, Ezaz T, et al: Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature 523:79-82 (2015).
15.
Kawagoshi T, Uno Y, Matsubara K, Matsuda Y, Nishida C: The ZW micro-sex chromosomes of the Chinese soft-shelled turtle (Pelodiscus sinensis, Trionychidae, Testudines) have the same origin as chicken chromosome 15. Cytogenet Genome Res 125:125-131 (2009).
16.
Keinath MC, Timoshevskiy VA, Timoshevskaya NY, Tsonis PA, Voss SR, Smith JJ: Initial characterization of the large genome of the salamander Ambystoma mexicanum using shotgun and laser capture chromosome sequencing. Sci Rep 5:16413 (2015).
17.
Kichigin IG, Giovannotti M, Makunin AI, Ng BL, Kabilov ML, 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).
18.
Kvikstad EM, Makova K: Rapid evolution of genes on the human X chromosome. eLS DOI: 10.1002/9780470015902.a0020858.pub2 (2013).
19.
Lisachov AP, Trifonov VA, Giovannotti M, Ferguson-Smith MA, Borodin PM: Heteromorphism of “homomorphic” sex chromosomes in two anole species (Squamata, Dactyloidae) revealed by synaptonemal complex analysis. Cytogenet Genome Res 151:89-95 (2017).
20.
Makunin AI, Kichigin IG, Larkin DM, O'Brien PC, Ferguson-Smith MA, et al: Contrasting origin of B chromosomes in two cervids (Siberian roe deer and grey brocket deer) unravelled by chromosome-specific DNA sequencing. BMC Genomics 17:618 (2016).
21.
Mangs AH, Morris BJ: The human pseudoautosomal region (PAR): origin, function and future. Curr Genomics 8:129-136 (2007).
22.
Marin R, Cortez D, Lamanna F, Pradeepa MM, Leushkin E, et al: Convergent origination of a Drosophila-like dosage compensation mechanism in a reptile lineage. Genome Res 27:1974-1987 (2017).
23.
Meisel RP, Connallon T: The faster-X effect: integrating theory and data. Trends Genet 29:537-544 (2013).
24.
Nicholson KE, Crother BI, Guyer C, Savage JM: It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa 3477:1-108 (2012)
25.
Poe S: 1986 Redux: new genera of anoles (Squamata: Dactyloidae) are unwarranted. Zootaxa 3626:295-299 (2013).
26.
Poe S, Nieto-Montes de Oca A, Torres-Carvajal O, De Queiroz K, Velasco JA, et al: A phylogenetic, biogeographic, and taxonomic study of all extant species of Anolis (Squamata; Iguanidae). Syst Biol 66:663-697 (2017).
27.
Rens W, O' Brien PCM, Yang F, Graves JAM, Ferguson-Smith MA: Karyotype relationships between four distantly related marsupials revealed by reciprocal chromosome painting. Chromosome Res 7:461-474 (1999).
28.
Rens W, Fu B, O'Brien PCM, Ferguson-Smith MA: Cross-species chromosome painting. Nat Protoc 1:783-790 (2006).
29.
Rovatsos M, Pokorná M, Altmanová M, Kratochvíl L: Cretaceous park of sex determination: sex chromosomes are conserved across iguanas. Biol Lett 10:20131093 (2014).
30.
Rovatsos M, Vukić J, Lymberakis P, Kratochvíl L: Evolutionary stability of sex chromosomes in snakes. Proc Biol Sci 282:20151992 (2015).
31.
Rovatsos M, Vukić J, Altmanová M, Johnson Pokorná M, Moravec J, Kratochvíl L: Conservation of sex chromosomes in lacertid lizards. Mol Ecol 25:3120-3126 (2016).
32.
Telenius H, Ponder BA, Tunnacliffe A, Pelmear AH, Carter NP, et al: Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4:257-263 (1992).
33.
Tomaszkiewicz M, Rangavittal S, Cechova M, Campos Sanchez R, Fescemyer HW, et al: A time- and cost-effective strategy to sequence mammalian Y chromosomes: an application to the de novo assembly of gorilla Y. Genome Res 26:530-540 (2016).
34.
Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D: Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 11:e1001643 (2013).
35.
Wilson MA, Makova KD: Evolution and survival on eutherian sex chromosomes. PLoS Genet 5:e1000568 (2009).
36.
Yang F, Carter NP, Shi L, Ferguson-Smith MA: A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103:642-652 (1995).
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