Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule

. 2021 Feb 04 ; 11 (1) : 3152. [epub] 20210204

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33542477
Odkazy

PubMed 33542477
PubMed Central PMC7862234
DOI 10.1038/s41598-021-82859-0
PII: 10.1038/s41598-021-82859-0
Knihovny.cz E-zdroje

Chromosome structural change has long been considered important in the evolution of post-zygotic reproductive isolation. The premise that karyotypic variation can serve as a possible barrier to gene flow is founded on the expectation that heterozygotes for structurally distinct chromosomal forms would be partially sterile (negatively heterotic) or show reduced recombination. We report the outcome of a detailed comparative molecular cytogenetic study of three antelope species, genus Raphicerus, that have undergone a rapid radiation. The species are largely conserved with respect to their euchromatic regions but the X chromosomes, in marked contrast, show distinct patterns of heterochromatic amplification and localization of repeats that have occurred independently in each lineage. We argue a novel hypothesis that postulates that the expansion of heterochromatic blocks in the homogametic sex can, with certain conditions, contribute to post-zygotic isolation. i.e., female hybrid incompatibility, the converse of Haldane's rule. This is based on the expectation that hybrids incur a selective disadvantage due to impaired meiosis resulting from the meiotic checkpoint network's surveillance of the asymmetric expansions of heterochromatic blocks in the homogametic sex. Asynapsis of these heterochromatic regions would result in meiotic silencing of unsynapsed chromatin and, if this persists, germline apoptosis and female infertility.

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White M. Animal Cytology and Evolution. London: Cambridge Univ. Press; 1973.

King M. Species evolution: The role of chromosome change. Cambridge: Cambridge Univ. Press; 1993.

Ayala FJ, Coluzzi M. Chromosome speciation: humans, Drosophila, and mosquitoes. Proc. Natl. Acad. Sci. USA. 2005;102:6535–6542. doi: 10.1073/pnas.0501847102. PubMed DOI PMC

Haldane JBS. Sex ratio and unisexual sterility in hybrid animals. J. Genetics. 1922;12:101–109. doi: 10.1007/BF02983075. DOI

Navarro A, Barton NH. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution. 2003;57:447–459. doi: 10.1111/j.0014-3820.2003.tb01537.x. PubMed DOI

Faria R, Navarro A. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 2010;25:660–669. doi: 10.1016/j.tree.2010.07.008. PubMed DOI

Brown JD, O’Neill RJ. Chromosomes, conflict, and epigenetics: Chromosomal speciation revisited. Annu. Rev. Genomics Hum. Genet. 2010;11:291–316. doi: 10.1146/annurev-genom-082509-141554. PubMed DOI

Wellenreuther M, Bernatchez L. Eco-evolutionary genomics of chromosomal inversions. Trends Ecol. Evol. 2018;33:427–440. doi: 10.1016/j.tree.2018.04.002. PubMed DOI

Faria R, Johannesson K, Butlin RK, Westram AM. Evolving inversions. Trends Ecol. Evol. 2019;34:239–248. doi: 10.1016/j.tree.2018.12.005. PubMed DOI

Besansky NJ, Krzywinski J, Lehmann T, Simard F, Kern M, Mukabayire O, Fontenille D, Touré Y, Sagnon N. Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. Proc. Natl. Acad. Sci. USA. 2003;100:10818–10823. doi: 10.1073/pnas.1434337100. PubMed DOI PMC

Borodin PM, Karamysheva TV, Belonogova NM, Torgasheva AA, Rubtsov NB, Searle JB. Recombination map of the common shrew, Sorex araneus (Eulipotyphla, Mammalia) Genetics. 2008;178:621–632. doi: 10.1534/genetics.107.079665. PubMed DOI PMC

Jones FC, et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature. 2012;484:55–61. doi: 10.1038/nature10944. PubMed DOI PMC

Farré M, Micheletti D, Ruiz-Herrera A. Recombination rates and genomic shuffling in human and chimpanzee: A new twist in the chromosomal speciation theory. Mol. Biol. Evol. 2013;30:853–864. doi: 10.1093/molbev/mss272. PubMed DOI PMC

Huang K, Rieseberg LH. Frequency, origins, and evolutionary role of chromosomal inversions in plants. Front. Plant. Sci. 2020;11:296. doi: 10.3389/fpls.2020.00296. PubMed DOI PMC

Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science. 2009;323:373–375. doi: 10.1126/science.1163601. PubMed DOI

Oliver PL, et al. Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet. 2009;5:1–14. doi: 10.1371/journal.pgen.1000753. PubMed DOI PMC

Noor MAF, Grams KL, Bertucci LA, Reiland J. Chromosomal inversions and the reproductive isolation of species. Proc. Natl Acad. Sci. USA. 2001;98:12084–12088. doi: 10.1073/pnas.221274498. PubMed DOI PMC

O’Neill RJ, Eldridge MD, Metcalfe CJ. Centromere dynamics and chromosome evolution in marsupials. J. Hered. 2004;95:375–381. doi: 10.1093/jhered/esh063. PubMed DOI

Ferree PM, Barbash DA. Species-Specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol. 2009;7:e1000234. doi: 10.1371/journal.pbio.1000234. PubMed DOI PMC

Hughes SE, Hawley RS. Heterochromatin: a rapidly evolving species barrier. PLoS Biol. 2009;7:e1000233. doi: 10.1371/journal.pbio.1000233. PubMed DOI PMC

O’Neill MJ, O’Neill RJ. Sex chromosome repeats tip the balance towards speciation. Mol. Ecol. 2018;27:3783–3798. doi: 10.1111/mec.14577. PubMed DOI

Dover GA, Strachan T, Coen ES, Brown SD. Molecular drive. Science. 1982;218:1069. doi: 10.1126/science.7146895. PubMed DOI

Charlesworth B, Jarne P, Assimacopoulos S. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin. Genet. Res. 1994;64:183–197. doi: 10.1017/S0016672300032845. PubMed DOI

Ugarkovic D, Plohl M. Variation in satellite DNA profiles-causes and effects. EMBO J. 2002;21:5955–5959. doi: 10.1093/emboj/cdf612. PubMed DOI PMC

Garrido-Ramos MA. Satellite DNA: An evolving topic. Genes. 2017;8:230. doi: 10.3390/genes8090230. PubMed DOI PMC

Escudeiro A, Adega F, Robinson TJ, Heslop-Harrison JS, Chaves R. Conservation, divergence, and functions of centromeric satellite DNA families in the Bovidae. Genome Biol. Evol. 2019;11:1152–1165. doi: 10.1093/gbe/evz061. PubMed DOI PMC

Robinson TJ, Ropiquet A. Examination of hemiplasy, homoplasy and phylogenetic discordance in chromosomal evolution of the Bovidae. Syst. Biol. 2011;60:439–450. doi: 10.1093/sysbio/syr045. PubMed DOI

Rubes J, Musilova P, Kopecna O, Kubickova S, Cernohorska H, Kulemsina AI. Comparative molecular cytogenetics in Cetartiodactyla. Cytogenet. Genome Res. 2012;137:194–207. doi: 10.1159/000338932. PubMed DOI

Gallagher DS, Davis SK, De Donato M, Burzlaff JD, Womack JE, Taylor JF, Kumamoto AT. A molecular cytogenetic analysis of the tribe Bovini (Artiodactyla: Bovidae: Bovinae) with an emphasis on sex chromosome morphology and NOR distribution. Chromosome Res. 1999;7:481–492. doi: 10.1023/A:1009254014526. PubMed DOI

Grubb, P. Genus Raphicerus: Grysboks, Steenbok in The Mammals of Africa Vol VI (eds. Kingdon, J. S. & Hoffmann, M.), 303. (Bloomsbury, London, UK, 2013).

Haltennorth T. Klassifikation der Saügertier: Artiodactyla I. Handbuch der Zoologie. 1963;8:1–167.

Haltenorth T, Diller H. A field guide to the Mammals of Africa including Madagascar. London: Collins; 1980.

Matthee CA, Robinson TJ. Cytochrome b phylogeny of the family bovidae: resolution within the Alcelaphini, Antilopini, Neotragini, and Tragelaphini. Mol. Phylogenet. Evol. 1999;12:31–46. doi: 10.1006/mpev.1998.0573. PubMed DOI

Matthee CA, Davis SK. Molecular insights into the evolution of the family Bovidae: A nuclear DNA perspective. Mol. Biol. Evol. 2001;18:1220–1230. doi: 10.1093/oxfordjournals.molbev.a003908. PubMed DOI

Bärmann E, Rössner G, Wörheide G. A revised phylogeny of Antilopini (Bovidae, Artiodactyla) using combined mitochondrial and nuclear genes. Mol. Phylogenet. Evol. 2013;67:484–493. doi: 10.1016/j.ympev.2013.02.015. PubMed DOI

Nguyen TT, Aniskin VM, Gerbault-Seureau M, Planton H, Renard JP, Nguyen BX, Hassanin A, Volobouev V. Phylogenetic position of the saola (Pseudoryx nghetinhensis) inferred from cytogenetic analysis of eleven species of Bovidae. Cytogenet. Genome Res. 2008;122:41–54. doi: 10.1159/000151315. PubMed DOI

Dobigny G, Ducroz J-F, Robinson TJ, Volobouev V. Cytogenetics and cladistics. Syst. Biol. 2004;53:470–484. doi: 10.1080/10635150490445698. PubMed DOI

Bulazel K, Ferreri GC, Eldridge MD, O’Neill RJ. Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol. 2007;8:R170. doi: 10.1186/gb-2007-8-8-r170. PubMed DOI PMC

D'Aiuto L, Barsanti P, Mauro S, Cserpan I, Lanave C, Ciccarese S. Physical relationship between satellite I and II DNA in centromeric regions of sheep chromosomes. Chromosome Res. 1997;5:375–381. doi: 10.1023/A:1018444325085. PubMed DOI

Cernohorska H, Kubickova S, Vahala J, Robinson TJ, Rubes J. Cytotype A of Kirk’s dik-dik (Madoqua kirkii) shows multiple tandem fusions. Cytogenet. Genome Res. 2011;132:255–263. doi: 10.1159/000322483. PubMed DOI

Cernohorska H, Kubickova S, Vahala J, Rubes J. Molecular insights into X;BTA5 chromosome rearrangements in the tribe Antilopini (Bovidae) Cytogenet. Genome Res. 2012;136:188–198. doi: 10.1159/000336248. PubMed DOI

Hayes H, Petit E, Dutrillaux B. Comparison of the RGB-banded karyotypes of cattle, sheep and goats. Cytogenet. Cell Genet. 1991;57:51–55. doi: 10.1159/000133114. PubMed DOI

Robinson TJ, Harrison WR, De León FAP, Davis SK, Elder FFB. A molecular cytogenetic analysis of X chromosome repatterning in the Bovidae: transpositions, inversions, and phylogenetic inference. Cytogenet. Cell Genet. 1998;80:179–184. doi: 10.1159/000014976. PubMed DOI

Iannuzzi L, Di Meo GP, Perucatti A, Incarnato D, Schibler L, Cribiu EP. Comparative FISH mapping of bovid X-chromosomes reveals homologies and divergences between the subfamilies Bovinae and Caprinae. Cytogenet. Cell Genet. 2000;89:171–176. doi: 10.1159/000015607. PubMed DOI

Chaves R, Guedes-Pinto H, Heslop-Harrison JS. Phylogenetic relationships and the primitive X chromosome inferred from chromosomal and satellite DNA analysis in Bovidae. Proc. R. Soc. B. 2005;272:2009–2016. doi: 10.1098/rspb.2005.3206. PubMed DOI PMC

Singh AP, Henschel S, Sperling K, Kalscheuer V, Neitzel H. Differences in the meiotic pairing behavior of gonosomal heterochromatin between female and male Microtus agrestis:implications for the mechanism of heterochromatin amplification on the X and Y. Cytogenet. Cell Genet. 2000;91:253–260. doi: 10.1159/000056854. PubMed DOI

Waddell PJ, Kishino H, Ota R. A phylogenetic foundation for comparative mammalian genomics. Genome Inform. 2001;12:141–154. doi: 10.11234/gi1990.12.141. PubMed DOI

Robinson TJ, Ruiz-Herrera A, Avise JC. Hemiplasy and homoplasy in the karyotypic phylogenies of mammals. Proc. Natl. Acad. Sci. USA. 2008;105:14477–14481. doi: 10.1073/pnas.0807433105. PubMed DOI PMC

Kingdon, J. Mammalian evolution in Africa in The Mammals of Africa Vol. 1. (eds. Kingdon, J., Happold, D.C.D., Butynski, T.M., Hoffmann, M., Happold, M. & Kalina, J.) 75–100. (Bloomsbury Publishing, London, 2013).

Lorenzen ED, Heller R, Siegismund HR. Comparative phylogeography of African savannah ungulates. Mol. Ecol. 2012;21:3656–3670. doi: 10.1111/j.1365-294X.2012.05650.x. PubMed DOI

Subramanian VV, Hochwagen A. The meiotic checkpoint network: step-by-step through meiotic prophase. Cold Spring Harb. Perspect. Biol. 2014;6:a016675. doi: 10.1101/cshperspect.a016675. PubMed DOI PMC

Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng C-X, Burgoyne PS. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet. 2005;37:41–47. doi: 10.1038/ng1484. PubMed DOI

Burgoyne PS, Mahadevaiah SK, Turner JM. The consequences of asynapsis for mammalian meiosis. Nat. Rev. Genet. 2009;10:207–216. doi: 10.1038/nrg2505. PubMed DOI

Turner JM. Meiotic silencing in mammals. Annu. Rev. Genet. 2015;49:395–412. doi: 10.1146/annurev-genet-112414-055145. PubMed DOI

Waters PD, Ruiz-Herrera A. Meiotic executioner genes protect the Y from extinction. Trends Genet. 2020;36:728–738. doi: 10.1016/j.tig.2020.06.008. PubMed DOI

Singh AP, Raman R. Mammalian sex chromosomes VI Synapsis in the heterochromatin-rich X chromosomes of four rodent species, Mus dunni, Bandicota bengalensis, Mesocricetus auratus, and Nesokia indica. Genome. 1993;36:195–198. doi: 10.1139/g93-026. PubMed DOI

Stack SM. Heterochromatin, the synaptonemal complex and crossing over. J. Cell Sci. 1984;71:159–176. PubMed

Micklejohn CD, Tau Y. Genetic conflict and sex chromosome evolution. Trends Ecol. Evol. 2009;25:223. doi: 10.1016/j.tree.2009.10.005. PubMed DOI PMC

Patten MM. Selfish X chromosomes and speciation. Mol. Ecol. 2018;27:3772–3782. doi: 10.1111/mec.14471. PubMed DOI

Pfeiffer, R.A. Cell cultures from blood and bone marrow in Methods in Human Cytogenetics (eds Schwarzacher, H.G., Wolf, U. & Passarge, E.) 1–28 (Springer-Verlag, Berlin, 1974).

Wolf, U. Cell cultures from tissue explants in Methods in Human Cytogenetics (eds Schwarzacher, H.G., Wolf, U. & Passarge, E.) 39–57 (Springer-Verlag, Berlin, 1974).

Schnedll, W. Banding patterns in human chromosomes visualized by Giemsa staining after various pretreatments in Methods in Human Cytogenetics (eds Schwarzacher, H.G., Wolf, U. & Passarge, E.) 95–117 (Springer-Verlag, Berlin, 1974).

ISCNDB. International System for Chromosome Nomenclature of Domestic Bovids (ISCNDB Cytogenet. Cell Genet. 2000;92:283–299. doi: 10.1159/000056917(2001). PubMed DOI

Kubickova S, Cernohorska H, Musilova P, Rubes J. The use of laser microdissection for the preparation of chromosome specific painting probes in farm animals. Chromosome Res. 2002;10:571–577. doi: 10.1023/A:1020914702767. PubMed DOI

Kopecna O, Kubickova S, Cernohorska H, Cabelova K, Vahala J, Martinkova N, Rubes J. Tribe-specific satellite DNA in non-domestic Bovidae. Chromosome Res. 2014;22:277–291. doi: 10.1007/s10577-014-9401-4. PubMed DOI

Cernohorska H, Kubickova S, Kopecna O, Vozdova M, Matthee CA, Robinson TJ, Rubes J. Nanger, Eudorcas, Gazella, and Antilope form a well-supported chromosomal clade within Antilopini (Bovidae, Cetartiodactyla) Chromosoma. 2015;124:235–247. doi: 10.1007/s00412-014-0494-5. PubMed DOI

Castley, G. & Lloyd, P. Raphicerus melanotis Cape Grysbok in The Mammals of Africa Vol VI (eds. Kingdon, J. S. & Hoffmann, M.), 304–307 (Bloomsbury, London, 2013).

du Toit, J.T. Raphicerus campestris Steenbok Grysbok in The Mammals of Africa Vol VI (eds. Kingdon, J. S. & Hoffmann, M.), 311–314 (Bloomsbury, London, 2013).

Hoffmann, M. & Wilson, V.J. Raphicerus sharpei Sharp’s Grysbok in The Mammals of Africa Vol VI (eds. Kingdon, J. S. & Hoffmann, M.), 308–310 (Bloomsbury, London, 2013).

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. 2024 Jan 25 ; 15 (2) : . [epub] 20240125

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