Genetic and karyotype divergence between parents affect clonality and sterility in hybrids
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
37930936
PubMed Central
PMC10627513
DOI
10.7554/elife.88366
PII: 88366
Knihovny.cz E-resources
- Keywords
- Cobitis, asexual reproduction, evolutionary biology, gametogenesis, hybrid sterility, hybridization, speciation, spined loaches,
- MeSH
- Phylogeny MeSH
- Hybridization, Genetic MeSH
- Infertility * MeSH
- Karyotype MeSH
- Humans MeSH
- Reproduction, Asexual * genetics MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Asexual reproduction can be triggered by interspecific hybridization, but its emergence is supposedly rare, relying on exceptional combinations of suitable genomes. To examine how genomic and karyotype divergence between parental lineages affect the incidence of asexual gametogenesis, we experimentally hybridized fishes (Cobitidae) across a broad phylogenetic spectrum, assessed by whole exome data. Gametogenic pathways generally followed a continuum from sexual reproduction in hybrids between closely related evolutionary lineages to sterile or inviable crosses between distant lineages. However, most crosses resulted in a combination of sterile males and asexually reproducing females. Their gametes usually experienced problems in chromosome pairing, but females also produced a certain proportion of oocytes with premeiotically duplicated genomes, enabling their development into clonal eggs. Interspecific hybridization may thus commonly affect cell cycles in a specific way, allowing the formation of unreduced oocytes. The emergence of asexual gametogenesis appears tightly linked to hybrid sterility and constitutes an inherent part of the extended speciation continuum.
Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czech Republic
Leibniz Institute of Freshwater Ecology and Inland Fisheries IGB Berlin Germany
Military Health Institute Military Medical Agency Prague Czech Republic
doi: 10.1101/2023.04.11.536494 PubMed
Update Ofdoi: 10.7554/eLife.88366.1 PubMed
Update Ofdoi: 10.7554/eLife.88366.2 PubMed
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Alberici da Barbiano L, Gompert Z, Aspbury AS, Gabor CR, Nice CC. Population genomics reveals a possible history of backcrossing and recombination in the gynogenetic fish Poecilia formosa. PNAS. 2013;110:13797–13802. doi: 10.1073/pnas.1303730110. PubMed DOI PMC
Auwera GV, O’Connor B. Genomics in the Cloud: Using Docker, GATK, and WDL in Terra. O’Reilly Media; 2020.
Balcova M, Faltusova B, Gergelits V, Bhattacharyya T, Mihola O, Trachtulec Z, Knopf C, Fotopulosova V, Chvatalova I, Gregorova S, Forejt J, Camerini-Otero RD. Hybrid Sterility Locus on Chromosome X Controls Meiotic Recombination Rate in Mouse. PLOS Genetics. 2016;12:e1005906. doi: 10.1371/journal.pgen.1005906. PubMed DOI PMC
Bates D, Maechler M, Bolker B, Walker S, Christensen RHB. Package ‘Lme4’. URL Httplme4 R-forge R-Proj. Lme4. 2009 https://lme4.r-forge.r-project.org/
Betto-Colliard C, Hofmann S, Sermier R, Perrin N, Stöck M. Profound genetic divergence and asymmetric parental genome contributions as hallmarks of hybrid speciation in polyploid toads. Proceedings. Biological Sciences. 2018;285:20172667. doi: 10.1098/rspb.2017.2667. PubMed DOI PMC
Bhattacharyya TT, Gregorova S, Mihola O, Anger M, Sebestova J, Denny P, Simecek P, Forejt J. Mechanistic basis of infertility of mouse intersubspecific hybrids. PNAS. 2013;110:E468–E477. doi: 10.1073/pnas.1219126110. PubMed DOI PMC
Bi K, Bogart JP. Probing the meiotic mechanism of intergenomic exchanges by genomic in situ hybridization on lampbrush chromosomes of unisexual Ambystoma (Amphibia: Caudata) Chromosome Research. 2010;18:371–382. doi: 10.1007/s10577-010-9121-3. PubMed DOI
Blokhina YP, Nguyen AD, Draper BW, Burgess SM. The telomere bouquet is a hub where meiotic double-strand breaks, synapsis, and stable homolog juxtaposition are coordinated in the zebrafish, Danio rerio. PLOS Genetics. 2019;15:e1007730. doi: 10.1371/journal.pgen.1007730. PubMed DOI PMC
Bohlen J, Li F, Šlechtová V. Phylogenetic Position of the Genus Bibarba as Revealed from Molecular Genetic Data (Teleostei Cobitidae) . Ichthyological Exploration of Freshwaters. 2019 doi: 10.23788/IEF-1099. DOI
Bouckaert RR. DensiTree: making sense of sets of phylogenetic trees. Bioinformatics. 2010;26:1372–1373. doi: 10.1093/bioinformatics/btq110. PubMed DOI
Brandvain Y, Pauly GB, May MR, Turelli M. Explaining Darwin’s corollary to Haldane’s rule: the role of mitonuclear interactions in asymmetric postzygotic isolation among toads. Genetics. 2014;197:743–747. doi: 10.1534/genetics.113.161133. PubMed DOI PMC
Bushnell B. BBMap: A Fast, Accurate, Splice-Aware Aligner. 2014. [October 28, 2022]. https://www.osti.gov/biblio/1241166
Castiglia R. Sympatric sister species in rodents are more chromosomally differentiated than allopatric ones: implications for the role of chromosomal rearrangements in speciation. Mammal Review. 2014;44:1–4. doi: 10.1111/mam.12009. DOI
Cataudella S, Sola L, Accame Muratori R, Capanna E. The chromosomes of 11 species of cyprinidae and one cobitidae from Italy, with some remarks on the problem of polyploidy in the cypriniformes. Genetica. 1977;47:161–171. doi: 10.1007/BF00123236. DOI
Charif D, Lobry JR. In: Structural Approaches to Sequence Evolution: Molecules, Networks, Populations. Bastolla U, Porto M, Roman HE, Vendruscolo M, editors. Springer; 2007. Seqinr 1.0-2: A contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis; pp. 207–232.
Choleva L, Janko K, De Gelas K, Bohlen J, Šlechtová V, Rábová M, Ráb P. Synthesis of clonality and polyploidy in vertebrate animals by hybridization between two sexual species. Evolution; International Journal of Organic Evolution. 2012;66:2191–2203. doi: 10.1111/j.1558-5646.2012.01589.x. PubMed DOI
Comeault AA, Matute DR. Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation. PNAS. 2018;115:9761–9766. doi: 10.1073/pnas.1809685115. PubMed DOI PMC
Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, Whitwham A, Keane T, McCarthy SA, Davies RM, Li H. Twelve years of SAMtools and BCFtools. GigaScience. 2021;10:giab008. doi: 10.1093/gigascience/giab008. PubMed DOI PMC
Dedukh D, Majtánová Z, Marta A, Pšenička M, Kotusz J, Klíma J, Juchno D, Boron A, Janko K. Parthenogenesis as a solution to hybrid sterility: The mechanistic basis of meiotic distortions in clonal and sterile hybrids. Genetics. 2020;215:975–987. doi: 10.1534/genetics.119.302988. PubMed DOI PMC
Dedukh D, Marta A, Janko K. Challenges and costs of asexuality: Variation in premeiotic genome duplication in gynogenetic hybrids from cobitis taenia complex. International Journal of Molecular Sciences. 2021;22:12117. doi: 10.3390/ijms222212117. PubMed DOI PMC
Dedukh D, Altmanová M, Klíma J, Kratochvíl L. Premeiotic endoreplication is essential for obligate parthenogenesis in geckos. Development. 2022a;149:dev200345. doi: 10.1242/dev.200345. PubMed DOI
Dedukh D, da Cruz I, Kneitz S, Marta A, Ormanns J, Tichopád T, Lu Y, Alsheimer M, Janko K, Schartl M. Achiasmatic meiosis in the unisexual Amazon molly, Poecilia formosa. Chromosome Research. 2022b;30:443–457. doi: 10.1007/s10577-022-09708-2. PubMed DOI PMC
Faria R, Navarro A. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends in Ecology & Evolution. 2010;25:660–669. doi: 10.1016/j.tree.2010.07.008. PubMed DOI
Ferree PM, Prasad S. How can satellite DNA divergence cause reproductive isolation? Let us count the chromosomal ways. Genetics Research International. 2012;2012:430136. doi: 10.1155/2012/430136. PubMed DOI PMC
Flajšhans M, Kohlmann K, Ráb P. Autotriploid tench Tinca tinca (L.) larvae obtained by fertilization of eggs previously subjected to postovulatory ageing in vitro and in vivo. Journal of Fish Biology. 2007;71:868–876. doi: 10.1111/j.1095-8649.2007.01557.x. DOI
Fox J, Friendly GG. The car package. R Found. Stat. Comput. 2007:1109–1431.
Fyon F, Berbel-Filho WM, Schlupp I, Wild G, Úbeda F. Why do hybrids turn down sex? Evolution; International Journal of Organic Evolution. 2023;77:2186–2199. doi: 10.1093/evolut/qpad129. PubMed DOI
Haldane JBS. Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics. 1922;12:101–109. doi: 10.1007/BF02983075. DOI
Hnátková E, Triantaphyllidis C, Ozouf-Costaz C, Majtánová Z, Bohlen J, Ráb P. Karyotype and chromosomal characteristics of rDNA of Cobitisstrumicae Karaman, 1955 (Teleostei, Cobitidae) from Lake Volvi, Greece. Comparative Cytogenetics. 2018;12:483–491. doi: 10.3897/CompCytogen.v12i4.28068. PubMed DOI PMC
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Molecular Biology and Evolution. 2018;35:518–522. doi: 10.1093/molbev/msx281. PubMed DOI PMC
Itono M, Morishima K, Fujimoto T, Bando E, Yamaha E, Arai K. Premeiotic endomitosis produces diploid eggs in the natural clone loach, Misgurnus anguillicaudatus (Teleostei: Cobitidae) Journal of Experimental Zoology. Part A, Comparative Experimental Biology. 2006;305:513–523. doi: 10.1002/jez.a.283. PubMed DOI
Iwai T, Sakai C, Konno F, Yamashita M. In: Medaka: A Model for Organogenesis, Human Disease and Evolution. Naruse K, Tanaka M, Takeda H, editors. Springer; 2011. Interspecific Medaka hybrids as experimental models for investigating cell division and germ cell development; pp. 287–304. DOI
Janko K, Vasil’eva ED, Ráb P, Rábová M, Šlechtová V, Vasil’eva E. Genetic and morphological analyses of 50-chromosome spined loaches (Cobitis, Cobitidae, Pisces) from the Black Sea basin that are morphologically similar to C. taenia, with the description of a new species. Folia Zool. Praha. 2005;54:405–420.
Janko K, Kotusz J, De Gelas K, Šlechtová V, Opoldusová Z, Drozd P, Choleva L, Popiołek M, Baláž M, Steinke D. Dynamic formation of asexual diploid and polyploid lineages: Multilocus analysis of cobitis reveals the mechanisms maintaining the diversity of clones. PLOS ONE. 2012;7:e45384. doi: 10.1371/journal.pone.0045384. PubMed DOI PMC
Janko K, Pačes J, Wilkinson-Herbots H, Costa RJ, Roslein J, Drozd P, Iakovenko N, Rídl J, Hroudová M, Kočí J, Reifová R, Šlechtová V, Choleva L. Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation. Molecular Ecology. 2018;27:248–263. doi: 10.1111/mec.14377. PubMed DOI PMC
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC
Kim IS, Lee JH. Diploid-triploid hybrid complex of the spined loach Cobitis sinesis and C.longicorpus (Pices, Cobitidae) Korean J Ichthyol. 1990;2:203–210.
Kim IS, Lee EH. Interspecific hybridization between triploid hybrid fish, Cobitis sinensis - longicorpus and two diploid species from Korea. Korean J Ichthyol. 1995;7:71–78.
Kim DS, Nam YK, Park IS. Survival and karyological analysis of reciprocal diploid and triploid hybrids between mud loach (Misgurnus mizolepis) and cyprinid loach (Misgurnus anguillicaudatus) Aquaculture. 1995;135:257–265. doi: 10.1016/0044-8486(95)01031-9. DOI
Kwan YS, Ko MH, Jeon YS, Kim HJ, Won YJ. Bidirectional mitochondrial introgression between Korean cobitid fish mediated by hybridogenetic hybrids. Ecology and Evolution. 2019;9:1244–1254. doi: 10.1002/ece3.4830. PubMed DOI PMC
Li H. Aligning Sequence Reads, Clone Sequences and Assembly Contigs with BWA-MEM. arXiv. 2013 https://arxiv.org/abs/1303.3997
Lutes AA, Neaves WB, Baumann DP, Wiegraebe W, Baumann P. Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature. 2010;464:283–286. doi: 10.1038/nature08818. PubMed DOI PMC
Macgregor HC, Uzzell TM. Gynogenesis in salamanders related to ambystoma jeffersonianum. Science. 1964;143:1043–1045. doi: 10.1126/science.143.3610.1043. PubMed DOI
Majtánová Z, Choleva L, Symonová R, Ráb P, Kotusz J, Pekárik L, Janko K. Asexual reproduction does not apparently increase the rate of chromosomal evolution: Karyotype stability in diploid and triploid clonal hybrid fish (cobitis, cypriniformes, teleostei) PLOS ONE. 2016;11:e0146872. doi: 10.1371/journal.pone.0146872. PubMed DOI PMC
Marta A, Dedukh D, Bartos O, Majtanova Z, Janko K. Cytogenetic Characterization of Seven Novel satDNA Markers in Two Species of Spined Loaches (Cobitis) and Their Clonal Hybrids. Genes. 2020;11:617. doi: 10.3390/genes11060617. PubMed DOI PMC
Minh BQ, Hahn MW, Lanfear R. New methods to calculate concordance factors for phylogenomic datasets. Molecular Biology and Evolution. 2020;37:2727–2733. doi: 10.1093/molbev/msaa106. PubMed DOI PMC
Morishima K, Nakamura-Shiokawa Y, Bando E, Li YJ, Boroń A, Khan MMR, Arai K. Cryptic clonal lineages and genetic diversity in the loach Misgurnus anguillicaudatus (Teleostei: Cobitidae) inferred from nuclear and mitochondrial DNA analyses. Genetica. 2008;132:159–171. doi: 10.1007/s10709-007-9158-1. PubMed DOI
Moritz C, Brown WM, Densmore LD, Wright JW, Vyas D, Donnellan S, Baverstock P. In: Evolution and Ecology of Unisexual Vertebrates. Dawley RM, Bogart JP, editors. Albany, NY: New York State Museum; 1989. Genetic diversity and the dynamics of hybrid Parthenogenesis in Cnemidophorus (Teiidae) and Heteronotia (Gekkonidae) pp. 87–112.
Murphy RW, Fu J, Macculloch RD, Darevsky IS, Kupriyanova LA. A fine line between sex and unisexuality: the phylogenetic constraints on parthenogenesis in lacertid lizards. Zoological Journal of the Linnean Society. 2000;130:527–549. doi: 10.1111/j.1096-3642.2000.tb02200.x. DOI
Neaves WB, Baumann P. Unisexual reproduction among vertebrates. Trends in Genetics. 2011;27:81–88. doi: 10.1016/j.tig.2010.12.002. PubMed DOI
Newton AA, Schnittker RR, Yu Z, Munday SS, Baumann DP, Neaves WB, Baumann P. Widespread failure to complete meiosis does not impair fecundity in parthenogenetic whiptail lizards. Development. 2016;143:4486–4494. doi: 10.1242/dev.141283. PubMed DOI PMC
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies. Molecular Biology and Evolution. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC
Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–528. doi: 10.1093/bioinformatics/bty633. PubMed DOI
Perdices A, Bohlen J, Šlechtová V, Doadrio I. Molecular Evidence for Multiple Origins of the European Spined Loaches (Teleostei, Cobitidae) PLOS ONE. 2016;11:e0144628. doi: 10.1371/journal.pone.0144628. PubMed DOI PMC
Potter S, Bragg JG, Blom MPK, Deakin JE, Kirkpatrick M, Eldridge MDB, Moritz C. Chromosomal speciation in the genomics era: Disentangling phylogenetic evolution of rock-wallabies. Frontiers in Genetics. 2017;8:10. doi: 10.3389/fgene.2017.00010. PubMed DOI PMC
Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841–842. doi: 10.1093/bioinformatics/btq033. PubMed DOI PMC
Rotelli MD, Policastro RA, Bolling AM, Killion AW, Weinberg AJ, Dixon MJ, Zentner GE, Walczak CE, Lilly MA, Calvi BR, Bosco G. A Cyclin A—Myb-MuvB—Aurora B network regulates the choice between mitotic cycles and polyploid endoreplication cycles. PLOS Genetics. 2019;15:e1008253. doi: 10.1371/journal.pgen.1008253. PubMed DOI PMC
Schwander T, Crespi BJ. Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality. Molecular Ecology. 2009;18:28–42. doi: 10.1111/j.1365-294X.2008.03992.x. PubMed DOI
Shaw KL, Mullen SP. Speciation continuum. The Journal of Heredity. 2014;105 Suppl 1:741–742. doi: 10.1093/jhered/esu060. PubMed DOI
Stankowski S, Ravinet M. Defining the speciation continuum. Evolution; International Journal of Organic Evolution. 2021;75:1256–1273. doi: 10.1111/evo.14215. PubMed DOI
Stelkens R, Seehausen O. Genetic distance between species predicts novel trait expression in their hybrids. Evolution; International Journal of Organic Evolution. 2009;63:884–897. doi: 10.1111/j.1558-5646.2008.00599.x. PubMed DOI
Stöck M, Lampert KP, Möller D, Schlupp I, Schartl M. Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa) Molecular Ecology. 2010;19:5204–5215. doi: 10.1111/j.1365-294X.2010.04869.x. PubMed DOI
Stöck M, Ustinova J, Betto-Colliard C, Schartl M, Moritz C, Perrin N. Simultaneous Mendelian and clonal genome transmission in a sexually reproducing, all-triploid vertebrate. Proceedings of the Royal Society B. 2012;279:1293–1299. doi: 10.1098/rspb.2011.1738. PubMed DOI PMC
Stöck M, Dedukh D, Reifová R, Lamatsch DK, Starostová Z, Janko K. Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum. Philosophical Transactions of the Royal Society B. 2021;376:20200103. doi: 10.1098/rstb.2020.0103. PubMed DOI PMC
Subramanian S, Ramasamy U, Chen D. VCF2PopTree: a client-side software to construct population phylogeny from genome-wide SNPs. PeerJ. 2019;7:e8213. doi: 10.7717/peerj.8213. PubMed DOI PMC
Sun F, Oliver-Bonet M, Liehr T, Starke H, Turek P, Ko E, Rademaker A, Martin RH. Variation in MLH1 distribution in recombination maps for individual chromosomes from human males. Human Molecular Genetics. 2006;15:2376–2391. doi: 10.1093/hmg/ddl162. PubMed DOI
Suzuki R. Hybridization experiments in cobitid fishes. The Japanese Journal of Genetics. 1957;32:8–14. doi: 10.1266/jjg.32.8. DOI
Suzuki A, Taki Y. Karyotype of a noemacheiline loach, Lefua echigonia. Jpn. J. Ichthyol. Jpn 1982
Tichopád T, Franěk R, Doležálková-Kaštánková M, Dedukh D, Marta A, Halačka K, Steinbach C, Janko K, Pšenička M. Clonal gametogenesis is triggered by intrinsic stimuli in the hybrid’s germ cells but is dependent on sex differentiation. Biology of Reproduction. 2022:446–457. doi: 10.1093/biolre/ioac074. PubMed DOI
Ueno K, Ojima Y. Diploid-tetraploid Complexes in the Genus Cobitis. Proceedings of the Japan Academy. 1976;52:446–449. doi: 10.2183/pjab1945.52.446. DOI
Welch JJ. Accumulating Dobzhansky-Muller incompatibilities: reconciling theory and data. Evolution; International Journal of Organic Evolution. 2004;58:1145–1156. doi: 10.1111/j.0014-3820.2004.tb01695.x. PubMed DOI
Yamashita M, Onozato H, Nakanishi T, Nagahama Y. Breakdown of the sperm nuclear envelope is a prerequisite for male pronucleus formation: direct evidence from the gynogenetic crucian carp Carassius auratus langsdorfii. Developmental Biology. 1990;137:155–160. doi: 10.1016/0012-1606(90)90016-c. PubMed DOI
Yoshikawa H, Xu D, Ino Y, Yoshino T, Hayashida T, Wang J, Yazawa R, Yoshizaki G, Takeuchi Y. Hybrid sterility in fish caused by mitotic arrest of primordial germ cells. Genetics. 2018;209:507–521. doi: 10.1534/genetics.118.300777. PubMed DOI PMC
Zhang C, Rabiee M, Sayyari E, Mirarab S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics. 2018;19:153. doi: 10.1186/s12859-018-2129-y. PubMed DOI PMC
A cyclical switch of gametogenic pathways in hybrids depends on the ploidy level
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