Landscape of snake' sex chromosomes evolution spanning 85 MYR reveals ancestry of sequences despite distinct evolutionary trajectories.

Tytuł:: Landscape of snake' sex chromosomes evolution spanning 85 MYR reveals ancestry of sequences despite distinct evolutionary trajectories.
Autorzy:: Viana PF; Coordenação de Biodiversidade, Laboratory of Animal Genetics, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo 2936, Petrópolis, Manaus, AM, 69067-375, Brazil. .
Ezaz T; Institute for Applied Ecology, Faculty of Science and Technology, University of Canberra, ACT 12, Canberra, 2616, Australia.
de Bello Cioffi M; Departamento de Genética e Evolução, Universidade Federal de São Carlos, São Carlos, SP, Brazil.; Institute of Human Genetics, University Hospital Jena, Am Klinikum 1, 07747, Jena, Germany.
Liehr T; Institute of Human Genetics, University Hospital Jena, Am Klinikum 1, 07747, Jena, Germany.
Al-Rikabi A; Institute of Human Genetics, University Hospital Jena, Am Klinikum 1, 07747, Jena, Germany.
Goll LG; Coordenação de Biodiversidade, Laboratory of Animal Genetics, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo 2936, Petrópolis, Manaus, AM, 69067-375, Brazil.
Rocha AM; Faculdade Cathedral, Laboratório de Zoologia Aplicada de Vertebrados Terrestres E Aquáticos, Av. Luis Canuto Chaves 293, Boa Vista, RR, Brazil.
Feldberg E; Coordenação de Biodiversidade, Laboratory of Animal Genetics, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo 2936, Petrópolis, Manaus, AM, 69067-375, Brazil.
Źródło:: Scientific reports [Sci Rep] 2020 Jul 27; Vol. 10 (1), pp. 12499. Date of Electronic Publication: 2020 Jul 27.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: London : Nature Publishing Group, copyright 2011-
MeSH Terms:: Evolution, Molecular*
Phylogeny*
Sex Chromosomes/*genetics
Snakes/*genetics
Animals ; Chromosome Painting ; Chromosomes, Artificial, Bacterial/genetics ; Comparative Genomic Hybridization ; DNA/genetics ; Female ; Genome ; Heterochromatin/genetics ; Male ; Species Specificity
References:: Gamble, T. et al. Restriction site-associated DNA sequencing (RAD-seq) reveals an extraordinary number of transitions among gecko sex-determining systems. Mol. Biol. Evol. 32(5), 1296–1309 (2015). (PMID: 25657328)
Ezaz, T., Srikulnath, K. & Graves, J. A. M. Origin of amniote sex chromosomes: An ancestral super-sex chromosome, or common requirements?. J. Hered. 108(1), 94–105 (2016). (PMID: 27634536)
Alam, S. M. I. et al. Did lizards follow unique pathways in sex chromosome evolution?. Genes 9(5), 239 (2018). (PMID: 5977179)
Pennell, M. W., Mank, J. E. & Peichel, C. L. Transitions in sex determination and sex chromosomes across vertebrate species. Mol. Ecol. 27(19), 3950–3963 (2018). (PMID: 294517156095824)
Deakin, J. E. & Ezaz, T. Understanding the evolution of reptile chromosomes through applications of combined cytogenetics and genomics approaches. Cytogenet. Genome Res. 157(1–2), 7–20 (2019). (PMID: 30645998)
Bull, J. J. Sex determination in reptiles. Q. Rev. Biol. 55(1), 3–21 (1980).
Bull, J. J. Evolution of sex determining mechanisms (The Benjamin/Cummings Press. Company, Menlo Park, 1983).
Janzen, F. J. & Paukstis, G. L. Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q. Rev. Biol. 66(2), 149–179 (1991). (PMID: 1891591)
Bachtrog, D. et al. Sex determination: Why so many ways of doing it?. Plos Biol. 12(7), e1001899 (2014). (PMID: 249834654077654)
Moritz, C. The evolution of a highly variable sex chromosome in Gehyra purpurascens (Gekkonidae). Chromosoma 90(2), 111–119 (1984).
Ezaz, T. et al. Relationships between vertebrate ZW and XY sex chromosome systems. Curr. Biol. 16(17), R736–R743 (2006). (PMID: 16950100)
Ezaz, T. et al. The ZW sex microchromosomes of an australian dragon lizard share no homology with those of other reptiles or birds. Chromosome Res. 17(8), 965 (2009). (PMID: 19967443)
Pokorná, M. & Kratochvíl, L. Phylogeny of sex-determining mechanisms in squamate reptiles: Are sex chromosomes an evolutionary trap?. Zool. J. Linn. Soc. 156(1), 168–183 (2009).
Sarre, S. D., Ezaz, T. & Georges, A. Transitions between sex-determining systems in reptiles and amphibians. Annu. Rev. Genomics Hum. Genet. 12, 391–406 (2011). (PMID: 21801024)
Holleley, C. E. et al. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature 523(7558), 79 (2015). (PMID: 26135451)
Rovatsos, M. et al. Mixed-up sex chromosomes: Identification of sex chromosomes in the X1X1X2X2/X1X2Y system of the legless lizards of the genus Lialis (Squamata: Gekkota: Pygopodidae). Cytogenet. Genome Res. 149(4), 282–289 (2016). (PMID: 27764831)
Radder, R. S. et al. Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol. Lett. 4(2), 176–178 (2007). (PMID: 2429925)
Quinn, A. E. et al. Evolutionary transitions between mechanisms of sex determination in vertebrates. Biol. Lett. 7(3), 443–448 (2011). (PMID: 212121043097877)
Deakin, J. E. 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(1), 447 (2016). (PMID: 272869594902969)
Montiel, E. E. et al. Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles. Chromosoma 126(1), 105–113 (2017). (PMID: 26842819)
Rovatsos, M. et al. Shared ancient sex chromosomes in varanids, beaded lizards and alligator lizards. Mol. Biol. Evol. 36(6), 1113–1120 (2019). (PMID: 30722046)
Rovatsos, M. et al. The rise and fall of differentiated sex chromosomes in geckos. Mol. Ecol. 28(12), 3042–3052 (2019). (PMID: 31063656)
Beçak, W. & Beçak, M. L. Cytotaxonomy and chromosomal evolution in Serpentes. Cytogenet. Genome Res. 8(4), 247–262 (1969).
Augstenová, B. et al. Evolutionary dynamics of the W chromosome in caenophidian snakes. Genes 9(1), 5 (2017). (PMID: 5793158)
Viana, P. F. et al. Evolutionary insights of the ZW sex chromosomes in snakes: A new chapter added by the amazonian puffing snakes of the genus Spilotes. Genes 10(4), 288 (2019).
Gamble, T. et al. The discovery of XY sex chromosomes in a boa and python. Curr. Biol. 27(14), 2148–2153 (2017). (PMID: 28690112)
Matsubara, K. et al. Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. P. Natl. Acad. Sci. 103(48), 18190–18195 (2006).
Rovatsos, M. et al. Evolutionary stability of sex chromosomes in snakes. P. R. Soc. B. 282(1821), 20151992 (2015).
Singchat, W. et al. Chromosome map of the siamese cobra: Did partial synteny of sex chromosomes in the amniote represent “a hypothetical ancestral super-sex chromosome” or random distribution?. BMC Genomics. 19(1), 939 (2018). (PMID: 305585336296137)
Singh, L. Evolution of karyotypes in snakes. Chromosoma 38(2), 185–236 (1972). (PMID: 5066447)
Viana, P. F. et al. Is the karyotype of neotropical boid snakes really conserved? Cytotaxonomy, chromosomal rearrangements and karyotype organization in the Boidae family. PLoS ONE 11(8), e0160274 (2016). (PMID: 274944094975421)
Augstenová, B. et al. ZW, XY, and yet ZW: Sex chromosome evolution in snakes even more complicated. Evolution 72(8), 1701–1707 (2018).
Augstenová, B. et al. Cytogenetic analysis did not reveal differentiated sex chromosomes in ten species of boas and pythons (Reptilia: Serpentes). Genes. 10(11), 934 (2019). (PMID: 6896069)
Matsubara, K. et al. Molecular cloning and characterization of satellite DNA sequences from constitutive heterochromatin of the habu snake (Protobothrops flavoviridis, Viperidae) and the burmese python (Python bivittatus, Pythonidae). Chromosoma 124(4), 529–539 (2015). (PMID: 26205503)
Matsubara, K. et al. Sex chromosome evolution in snakes inferred from divergence patterns of two gametologous genes and chromosome distribution of sex chromosome-linked repetitive sequences. Zool. Lett. 2(1), 19 (2016).
Beçak, W. Constituição cromossômica e mecanismo de determinação do sexo em ofidios sulamericanos. I. Aspectos cariotipicos. Mem. Inst. Butantan. 32, 37–78 (1965). (PMID: 5895361)
Nery, M. D. A. et al. Karyotype of Philodryas nattereri and Philodryas olfersii with a comparative analysis of the Dipsadidae family. Genet. Mol. Res. 14(2), 6297–6302 (2015). (PMID: 26125832)
Falcione, C., Hernando, A. & Bressa, M. J. Comparative cytogenetic analysis in Erythrolamprus snakes (Serpentes: Dipsadidae) from Argentina. An. Acad. Bras. Cienc. 90(2), 1417–1429 (2018). (PMID: 29898102)
De Smet, W. H. The chromosomes of 23 species of snakes. Acta Zool. Pathol. Antverp. 70, 85–118 (1978).
Singh, L., Purdom, I. F. & Jones, K. W. Sex chromosome associated satellite DNA: Evolution and conservation. Chromosoma 79(2), 137–157 (1980). (PMID: 7398495)
Aprea, G. et al. The karyology of Vipera aspis, V. atra, V. hugyi, and Cerastes vipera. Amphibia-Reptilia. 27(1), 113–119 (2006).
Matsubara, K. et al. Karyotype analysis of four blind snake species (Reptilia: Squamata: Scolecophidia) and karyotypic changes in Serpentes. Cytogenet. Genome Res. 157(1–2), 98–106 (2019). (PMID: 30754040)
Singh, L., Sharma, T. & Ray-Chaudhuri, S. P. Multiple sex-chromosomes in the common Indian krait, Bungarus caeruleus. Schneider. Chromosoma. 31(4), 386–391 (1970). (PMID: 5490305)
Singh, L. Multiple W chromosome in a sea snake, Enhydrina schistosa daudin. Experientia 28(1), 95–97 (1972).
Freitas, N. L. et al. Early stages of XY sex chromosomes differentiation in the fish Hoplias malabaricus (Characiformes, Erythrinidae) revealed by DNA repeats accumulation. Curr. Genomics. 19(3), 216–226 (2018).
Sember, A. et al. Sex chromosome evolution and genomic divergence in the fish Hoplias malabaricus (Characiformes, Erythrinidae). Front. Genet. 9, 71 (2018). (PMID: 295562495845122)
Shams, F. et al. Karyotypes and sex chromosomes in two australian native freshwater fishes, golden perch (Macquaria ambigua) and murray cod (Maccullochella peelii) (Percichthyidae). Int. J. Mol. Sci. 20(17), 4244 (2019). (PMID: 6747191)
Abramyan, J. et al. Z and W sex chromosomes in the cane toad (Bufo marinus). Chromosome Res. 17(8), 1015 (2009). (PMID: 19936947)
Keinath, M. C. et al. Miniscule differences between sex chromosomes in the giant genome of a salamander. Sci. Rep-UK 8(1), 17882 (2018).
Ezaz, T. et al. The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosome Res. 13(8), 763–776 (2005). (PMID: 16331408)
Ezaz, T. et al. An XX/XY sex microchromosome system in a freshwater turtle, Chelodina longicollis (Testudines: Chelidae) with genetic sex determination. Chromosome Res. 14(2), 139–150 (2006). (PMID: 16544188)
Ezaz, T. et al. Sequence and gene content of a large fragment of a lizard sex chromosome and evaluation of candidate sex differentiating gene R-spondin 1. BMC Genom. 14(1), 899 (2013).
Young, M. J. et al. Molecular cytogenetic map of the central bearded dragon, Pogona vitticeps (Squamata: Agamidae). Chromosome Res. 21(4), 361–374 (2013). (PMID: 23703235)
Ezaz, T. et al. Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet. Genome Res. 127(2–4), 249–260 (2009). (PMID: 20332599)
Rovatsos, M. et al. Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards. Sci. Rep. 9(1), 7832 (2019). (PMID: 311271346534595)
Ogata, M. et al. Reconstruction of female heterogamety from admixture of XX–XY and ZZ–ZW sex-chromosome systems within a frog species. Mol. Ecol. 27(20), 4078–4089 (2018). (PMID: 30086193)
Traut, W. & Winking, H. Meiotic chromosomes and stages of sex chromosome evolution in fish: Zebrafish, platyfish and guppy. Chromosome Res. 9(8), 659–672 (2001). (PMID: 11778689)
de Moraes, R. L. R. et al. Comparative cytogenetics and neo-Y formation in small-sized fish species of the genus Pyrrhulina (Characiformes, Lebiasinidae). Front. Genet. 10, 678 (2019). (PMID: 314281276689988)
Gazoni, T. et al. More sex chromosomes than autosomes in the amazonian frog Leptodactylus pentadactylus. Chromosoma 127(2), 269–278 (2018). (PMID: 29372309)
O’Meally, D. et al. Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Res. 18(7), 787–800 (2010). (PMID: 20734128)
Srikulnath, K. et al. Karyotypic evolution in squamate reptiles: comparative gene mapping revealed highly conserved linkage homology between the butterfly lizard (Leiolepis reevesii rubritaeniata, Agamidae, Lacertilia) and the japanese four-striped rat snake (Elaphe quadrivirgata, Colubridae, Serpentes). Chromosome Res. 17(8), 975 (2009). (PMID: 19937109)
Pokorná, M. et al. Strong conservation of the bird Z chromosome in reptilian genomes is revealed by comparative painting despite 275 million years divergence. Chromosoma 120(5), 455 (2011). (PMID: 21725690)
Ezaz, T. & Deakin, J. E. Repetitive sequence and sex chromosome evolution in vertebrates. Adv. Evol. Biol. 2014, 1–9 (2014).
Hsiang, A. Y. et al. The origin of snakes: Revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evol. Biol. 15(1), 87 (2015). (PMID: 259897954438441)
Harrington, S. M. & Reeder, T. W. Phylogenetic inference and divergence dating of snakes using molecules, morphology and fossils: new insights into convergent evolution of feeding morphology and limb reduction. Biol. J. Linn. Soc. 121(2), 379–394 (2017).
Lippman, Z. et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476 (2004). (PMID: 15269773)
Chalopin, D. Transposable elements and early evolution of sex chromosomes in fish. Chromosome Res. 23, 545–560 (2015). (PMID: 26429387)
Li, S. F. et al. Repetitive sequences and epigenetic modification: inseparable partners play important roles in the evolution of plant sex chromosomes. Planta 243, 1083–1095 (2016). (PMID: 26919983)
Viana, P. F. et al. An optimized protocol for obtaining mitotic chromosomes from cultured reptilian lymphocytes. Nucleus 59(3), 191–195 (2016).
Matsubara, K. et al. Non-homologous sex chromosomes in two geckos (Gekkonidae: Gekkota) with female heterogamety. Cytogenet. Genome Res. 143(4), 251–258 (2014). (PMID: 25227445)
Zwick, M. S. et al. A rapid procedure for the isolation of C 0 t–1 DNA from plants. Genome 40(1), 138–142 (1997). (PMID: 18464813)
Symonová, R. et al. Characterization of fish genomes by GISH and CGH. In Fish Cytogenetic Techniques Ray-Fin Fishes and Chondrichthyans (eds Ozouf-Costaz, C. et al.) 118–131 (CCR Press, Boca Raton, 2015).
Pyron, R. A., Reynolds, R. G. & Burbrink, F. T. A taxonomic revision of boas (Serpentes: Boidae). Zootaxa 3846(2), 249–260 (2014). (PMID: 25112250)
Reynolds, R. G., Niemiller, M. L. & Revell, L. J. Toward a Tree-of-Life for the boas and pythons: Multilocus species-level phylogeny with unprecedented taxon sampling. Mol. Phylogenet. Evol. 71, 201–213 (2014).
Figueroa, A. et al. A species-level phylogeny of extant snakes with description of a new colubrid subfamily and genus. PLoS ONE 11(9), e0161070 (2016). (PMID: 276032055014348)
Singchat, W. et al. Do sex chromosomes of snakes, monitor lizards, and iguanian lizards result from multiple fission of an “ancestral amniote super-sex chromosome”?. Chromosome Res. 28, 209–228 (2020). (PMID: 32358743)
Substance Nomenclature:: 0 (Heterochromatin)
9007-49-2 (DNA)
Entry Date(s):: Date Created: 20200729 Date Completed: 20201209 Latest Revision: 20210727
Update Code:: 20240104
PubMed Central ID:: PMC7385105
DOI:: 10.1038/s41598-020-69349-5
PMID:: 32719365
: Czasopismo naukowe

Pełny tekst

Most of snakes exhibit a ZZ/ZW sex chromosome system, with different stages of degeneration. However, undifferentiated sex chromosomes and unique Y sex-linked markers, suggest that an XY system has also evolved in ancestral lineages. Comparative cytogenetic mappings revealed that several genes share ancestry among X, Y and Z chromosomes, implying that XY and ZW may have undergone transitions during serpent's evolution. In this study, we performed a comparative cytogenetic analysis to identify homologies of sex chromosomes across ancestral (Henophidia) and more recent (Caenophidia) snakes. Our analysis suggests that, despite ~ 85 myr of independent evolution, henophidians and caenophidians retained conserved synteny over much of their genomes. However, our findings allowed us to discover that ancestral and recent lineages of snakes do not share the same sex chromosome and followed distinct pathways for sex chromosomes evolution.

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