{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,12]],"date-time":"2025-12-12T13:07:10Z","timestamp":1765544830406},"reference-count":99,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,1,6]],"date-time":"2022-01-06T00:00:00Z","timestamp":1641427200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,1,6]],"date-time":"2022-01-06T00:00:00Z","timestamp":1641427200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Genomics"],"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>The genetic basis of hybrid incompatibilities is characterized by pervasive cases of gene interactions. Sex chromosomes play a major role in speciation and X-linked hybrid male sterility (HMS) genes have been identified. Interestingly, some of these genes code for proteins with DNA binding domains, suggesting a capability to act as <jats:italic>trans<\/jats:italic>-regulatory elements and disturb the expression of a large number of gene targets. To understand how interactions between <jats:italic>trans<\/jats:italic>- and <jats:italic>cis<\/jats:italic>-regulatory elements contribute to speciation, we aimed to map putative X-linked <jats:italic>trans<\/jats:italic>-regulatory elements and to identify gene targets with disrupted gene expression in sterile hybrids between the subspecies <jats:italic>Drosophila pseudoobscura pseudoobscura<\/jats:italic> and <jats:italic>D. p. bogotana<\/jats:italic>.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>We find six putative <jats:italic>trans<\/jats:italic>-regulatory proteins within previously mapped X chromosome HMS loci with sequence changes that differentiate the two subspecies. Among them, the previously characterized HMS gene <jats:italic>Overdrive<\/jats:italic> (<jats:italic>Ovd<\/jats:italic>) had the largest number of amino acid changes between subspecies, with some substitutions localized within the protein\u2019s DNA binding domain. Using an introgression approach, we detected transcriptional responses associated with a sterility\/fertility <jats:italic>Ovd<\/jats:italic> allele swap. We found a network of 52 targets of Ovd and identified <jats:italic>cis<\/jats:italic>-regulatory effects among target genes with disrupted expression in sterile hybrids. However, a combined analysis of polymorphism and divergence in non-coding sequences immediately upstream of target genes found no evidence of changes in candidate regulatory proximal <jats:italic>cis<\/jats:italic>-elements. Finally, peptidases were over-represented among target genes.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>We provide evidence of divergence between subspecies within the DNA binding domain of the HMS protein Ovd and identify <jats:italic>trans<\/jats:italic> effects on the expression of 52 gene targets. Our results identify a network of <jats:italic>trans<\/jats:italic>-<jats:italic>cis<\/jats:italic> interactions with possible effects on HMS. This network provides molecular evidence of gene \u00d7 gene incompatibilities as contributors to hybrid dysfunction.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12864-021-08267-w","type":"journal-article","created":{"date-parts":[[2022,1,6]],"date-time":"2022-01-06T17:02:52Z","timestamp":1641488572000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Divergence of X-linked trans regulatory proteins and the misexpression of gene targets in sterile Drosophila pseudoobscura hybrids"],"prefix":"10.1186","volume":"23","author":[{"given":"Alwyn C.","family":"Go","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alberto","family":"Civetta","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,1,6]]},"reference":[{"key":"8267_CR1","volume-title":"Speciation","author":"J Coyne","year":"2004","unstructured":"Coyne J, Orr H. Speciation. Sunderland: Sinauer Associates; 2004."},{"key":"8267_CR2","doi-asserted-by":"publisher","first-page":"1501","DOI":"10.1126\/science.282.5393.1501","volume":"282","author":"CT Ting","year":"1998","unstructured":"Ting CT, Tsaur SC, Wu ML, Wu CI. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science. 1998;282:1501\u20134.","journal-title":"Science."},{"key":"8267_CR3","doi-asserted-by":"publisher","first-page":"1448","DOI":"10.1126\/science.1128721","volume":"313","author":"JP Masly","year":"2006","unstructured":"Masly JP, Jones CD, Noor MAF, Locke J, Orr HA. Gene transposition as a cause of hybrid sterility in Drosophila. Science. 2006;313:1448\u201350.","journal-title":"Science."},{"key":"8267_CR4","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1126\/science.1163934","volume":"323","author":"N Phadnis","year":"2009","unstructured":"Phadnis N, Orr HA. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science. 2009;323:376\u20139.","journal-title":"Science."},{"key":"8267_CR5","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1126\/science.1163601","volume":"323","author":"O Mihola","year":"2009","unstructured":"Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science. 2009;323:373\u20135.","journal-title":"Science."},{"key":"8267_CR6","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1093\/genetics\/140.1.201","volume":"140","author":"DE Perez","year":"1995","unstructured":"Perez DE, Wu CI. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: One gene is not enough. Genetics. 1995;140:201\u20136.","journal-title":"Genetics."},{"key":"8267_CR7","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1093\/genetics\/158.3.1089","volume":"158","author":"HA Orr","year":"2001","unstructured":"Orr HA, Irving S. Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics. 2001;158:1089\u2013100.","journal-title":"Genetics."},{"key":"8267_CR8","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1038\/nature01679","volume":"423","author":"DC Presgraves","year":"2003","unstructured":"Presgraves DC, Balagopalan L, Abmayr SM, Orr HA. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature. 2003;423:715\u20139.","journal-title":"Nature."},{"key":"8267_CR9","doi-asserted-by":"publisher","first-page":"1399","DOI":"10.1093\/genetics\/164.4.1399","volume":"164","author":"Y Tao","year":"2003","unstructured":"Tao Y, Zeng ZB, Li J, Hartl DL, Laurie CC. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. II. Mapping hybrid male sterility loci on the third chromosome. Genetics. 2003;164:1399\u2013418.","journal-title":"Genetics."},{"key":"8267_CR10","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1093\/genetics\/166.2.789","volume":"166","author":"K Sawamura","year":"2004","unstructured":"Sawamura K, Roote J, Wu CI, Yamamoto MT. Genetic Complexity Underlying Hybrid Male Sterility in Drosophila. Genetics. 2004;166:789\u201396.","journal-title":"Genetics."},{"key":"8267_CR11","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1111\/j.1558-5646.2009.00823.x","volume":"64","author":"AS Chang","year":"2010","unstructured":"Chang AS, Noor MAF. Epistasis modifies the dominance of loci causing hybrid male sterility in the Drosophila pseudoobscura species group. Evolution. 2010;64:253\u201360.","journal-title":"Evolution."},{"key":"8267_CR12","doi-asserted-by":"publisher","first-page":"1001","DOI":"10.1534\/genetics.111.132324","volume":"189","author":"N Phadnis","year":"2011","unstructured":"Phadnis N. Genetic architecture of male sterility and segregation distortion in Drosophila pseudoobscura bogota-USA hybrids. Genetics. 2011;189:1001\u20139.","journal-title":"Genetics."},{"key":"8267_CR13","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1266\/jjg.54.69","volume":"54","author":"Y Inoue","year":"1979","unstructured":"Inoue Y, Watanabe TK. Inversion polymorphisms in japanese natural populations of Drosophila melanogaster. Japanese J Genet. 1979;54:69\u201382.","journal-title":"Japanese J Genet"},{"key":"8267_CR14","doi-asserted-by":"publisher","first-page":"1747","DOI":"10.1093\/genetics\/154.4.1747","volume":"154","author":"DA Barbash","year":"2000","unstructured":"Barbash DA, Roote J, Ashburner M. The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids. Genetics. 2000;154:1747\u201371.","journal-title":"Genetics."},{"key":"8267_CR15","doi-asserted-by":"publisher","first-page":"5302","DOI":"10.1073\/pnas.0836927100","volume":"100","author":"DA Barbash","year":"2003","unstructured":"Barbash DA, Siino DF, Tarone AM, Roote J. A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci U S A. 2003;100:5302\u20137.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"8267_CR16","doi-asserted-by":"publisher","first-page":"1552","DOI":"10.1126\/science.aac7504","volume":"350","author":"N Phadnis","year":"2015","unstructured":"Phadnis N, Baker EP, Cooper JC, Frizzell KA, Hsieh E, de La Cruz AFA, et al. An essential cell cycle regulation gene causes hybrid inviability in Drosophila. Science. 2015;350:1552\u20135.","journal-title":"Science."},{"key":"8267_CR17","doi-asserted-by":"publisher","first-page":"e00476","DOI":"10.1128\/MCB.00476-17","volume":"38","author":"DG Baumann","year":"2018","unstructured":"Baumann DG, Dai M-S, Lu H, Gilmour DS. GFZF, a Glutathione S -Transferase Protein Implicated in Cell Cycle Regulation and Hybrid Inviability, Is a Transcriptional Coactivator. Mol Cell Biol. 2018;38:e00476\u201317.","journal-title":"Mol Cell Biol"},{"key":"8267_CR18","doi-asserted-by":"publisher","first-page":"1783","DOI":"10.1093\/molbev\/msz105","volume":"36","author":"JC Cooper","year":"2019","unstructured":"Cooper JC, Lukacs A, Reich S, Schauer T, Imhof A, Phadnis N, et al. Altered Localization of Hybrid Incompatibility Proteins in Drosophila. Mol Biol Evol. 2019;36:1783\u201392.","journal-title":"Mol Biol Evol"},{"key":"8267_CR19","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1093\/jhered\/esu003","volume":"105","author":"T Mor\u00e1n","year":"2014","unstructured":"Mor\u00e1n T, Fontdevila A. Genome-wide dissection of hybrid sterility in Drosophila confirms a polygenic threshold architecture. J Hered. 2014;105:381\u201396.","journal-title":"J Hered"},{"key":"8267_CR20","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.02504","volume":"3","author":"LM Turner","year":"2014","unstructured":"Turner LM, Harr B. Genome-wide mapping in a house mouse hybrid zone reveals hybrid sterility loci and Dobzhansky-Muller interactions. eLife. 2014;3:e02504.","journal-title":"eLife."},{"key":"8267_CR21","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1371\/journal.pgen.1004162","volume":"10","author":"LM Turner","year":"2014","unstructured":"Turner LM, White MA, Tautz D, Payseur BA. Genomic Networks of Hybrid Sterility. PLoS Genet. 2014;10:18\u201322.","journal-title":"PLoS Genet"},{"key":"8267_CR22","volume-title":"Hybrid Incompatibility in Drosophila: An Updated Genetic and Evolutionary Analysis","author":"A Fontdevila","year":"2016","unstructured":"Fontdevila A, eLS. Hybrid Incompatibility in Drosophila: An Updated Genetic and Evolutionary Analysis. Chichester: Wiley; 2016."},{"key":"8267_CR23","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1007\/BF02983075","volume":"12","author":"JBS Haldane","year":"1922","unstructured":"Haldane JBS. Sex ratio and unisexual sterility in hybrid animals. J Genet. 1922;12:101\u20139.","journal-title":"J Genet"},{"key":"8267_CR24","first-page":"180","volume-title":"Speciation and its consequences","author":"JAOH Coyne","year":"1989","unstructured":"Coyne JAOH. Two rules of speciation. In: Otte D, Endler J, editors. Speciation and its consequences. Sunderland: Sinauer Associates; 1989. p. 180\u2013207."},{"key":"8267_CR25","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1534\/genetics.105.052985","volume":"173","author":"AJ Moehring","year":"2006","unstructured":"Moehring AJ, Llopart A, Elwyn S, Coyne JA, Mackay TFC. The genetic basis of postzygotic reproductive isolation between Drosophila santomea and D. yakuba due to hybrid male sterility. Genetics. 2006;173:225\u201333.","journal-title":"Genetics."},{"key":"8267_CR26","doi-asserted-by":"publisher","first-page":"2213","DOI":"10.1534\/genetics.107.085340","volume":"179","author":"JM Good","year":"2008","unstructured":"Good JM, Dean MD, Nachman MW. A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics. 2008;179:2213\u201328.","journal-title":"Genetics."},{"key":"8267_CR27","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1038\/nature08441","volume":"461","author":"J Kitano","year":"2009","unstructured":"Kitano J, Ross JA, Mori S, Kume M, Jones FC, Chan YF, et al. A role for a neo-sex chromosome in stickleback speciation. Nature. 2009;461:1079\u201383.","journal-title":"Nature."},{"key":"8267_CR28","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003013","volume":"8","author":"RP Meisel","year":"2012","unstructured":"Meisel RP, Malone JH, Clark AG. Faster-X Evolution of Gene Expression in Drosophila. PLoS Genet. 2012;8:e1003013.","journal-title":"PLoS Genet"},{"key":"8267_CR29","doi-asserted-by":"publisher","first-page":"3873","DOI":"10.1093\/molbev\/mss190","volume":"29","author":"A Llopart","year":"2012","unstructured":"Llopart A. The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea, and their hybrids. Mol Biol Evol. 2012;29:3873\u201386.","journal-title":"Mol Biol Evol"},{"key":"8267_CR30","doi-asserted-by":"publisher","first-page":"2444","DOI":"10.1093\/gbe\/evu198","volume":"6","author":"D Garrigan","year":"2014","unstructured":"Garrigan D, Kingan SB, Geneva AJ, Vedanayagam JP, Presgraves DC. Genome diversity and divergence in Drosophila mauritiana: Multiple signatures of faster X evolution. Genome Biol Evol. 2014;6:2444\u201358.","journal-title":"Genome Biol Evol"},{"key":"8267_CR31","doi-asserted-by":"publisher","first-page":"3753","DOI":"10.1111\/mec.14534","volume":"27","author":"B Charlesworth","year":"2018","unstructured":"Charlesworth B, Campos JL, Jackson BC. Faster-X evolution: Theory and evidence from Drosophila. Mol Ecol. 2018;27:3753\u201371.","journal-title":"Mol Ecol"},{"key":"8267_CR32","doi-asserted-by":"publisher","first-page":"3811","DOI":"10.1111\/mec.14708","volume":"27","author":"A Llopart","year":"2018","unstructured":"Llopart A. Faster-X evolution of gene expression is driven by recessive adaptive cis-regulatory variation in Drosophila. Mol Ecol. 2018;27:3811\u201321.","journal-title":"Mol Ecol"},{"key":"8267_CR33","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.1093\/genetics\/147.3.1091","volume":"147","author":"RL Wang","year":"1997","unstructured":"Wang RL, Wakeley J, Hey J. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics. 1997;147:1091\u2013106.","journal-title":"Genetics."},{"key":"8267_CR34","doi-asserted-by":"publisher","first-page":"11976","DOI":"10.1038\/srep11976","volume":"5","author":"S Gomes","year":"2015","unstructured":"Gomes S, Civetta A. Hybrid male sterility and genome-wide misexpression of male reproductive proteases. Sci Rep. 2015;5:11976.","journal-title":"Sci Rep"},{"key":"8267_CR35","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1007\/s00239-016-9734-z","volume":"82","author":"A Civetta","year":"2016","unstructured":"Civetta A. Misregulation of Gene Expression and Sterility in Interspecies Hybrids: Causal Links and Alternative Hypotheses. J Mol Evol. 2016;82:176\u201382.","journal-title":"J Mol Evol"},{"key":"8267_CR36","doi-asserted-by":"publisher","first-page":"1601","DOI":"10.1534\/genetics.107.086074","volume":"179","author":"SW Schaeffer","year":"2008","unstructured":"Schaeffer SW, Bhutkar A, McAllister BF, Matsuda M, Matzkin LM, O\u2019Grady PM, et al. Polytene chromosomal maps of 11 drosophila species: The order of genomic scaffolds inferred from genetic and physical maps. Genetics. 2008;179:1601\u201355.","journal-title":"Genetics."},{"key":"8267_CR37","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0108267","volume":"9","author":"I Theofel","year":"2014","unstructured":"Theofel I, Bartkuhn M, Hundertmark T, Boettger T, G\u00e4rtner SMK, Leser K, et al. TBRD-1 selectively controls gene activity in the Drosophila testis and interacts with two new members of the bromodomain and extra-terminal (BET) family. PLoS One. 2014;9:e108267.","journal-title":"PLoS One"},{"key":"8267_CR38","first-page":"439","volume":"6","author":"I Theofel","year":"2017","unstructured":"Theofel I, Bartkuhn M, Boettger T, G\u00e4rtner SMK, Kreher J, Brehm A, et al. TBRD-1 and tBRD-2 regulate expression of genes necessary for spermatid differentiation. Biology Open. 2017;6:439\u201348.","journal-title":"Biology Open"},{"key":"8267_CR39","first-page":"1065","volume":"9","author":"D Alhazmi","year":"2019","unstructured":"Alhazmi D, Fudyk SK, Civetta A. Testes proteases expression and hybrid male sterility between subspecies of Drosophila pseudoobscura. G3: Genes, Genomes. Genetics. 2019;9:1065\u201374.","journal-title":"Genetics."},{"key":"8267_CR40","doi-asserted-by":"publisher","first-page":"W191","DOI":"10.1093\/nar\/gkz369","volume":"47","author":"U Raudvere","year":"2019","unstructured":"Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, et al. G:Profiler: A web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 2019;47:W191\u20138.","journal-title":"Nucleic Acids Res"},{"key":"8267_CR41","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1126\/science.1090005","volume":"188","author":"MC King","year":"1975","unstructured":"King MC, Wilson AC. Evolution at two levels in humans and chimpanzees. Science. 1975;188:107\u201316.","journal-title":"Science."},{"key":"8267_CR42","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/j.cell.2008.06.030","volume":"134","author":"SB Carroll","year":"2008","unstructured":"Carroll SB. Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution. Cell. 2008;134:25\u201336.","journal-title":"Cell."},{"key":"8267_CR43","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1038\/nature10532","volume":"478","author":"D Brawand","year":"2011","unstructured":"Brawand D, Soumillon M, Necsulea A, Julien P, Cs\u00e1rdi G, Harrigan P, et al. The evolution of gene expression levels in mammalian organs. Nature. 2011;478:343\u20138.","journal-title":"Nature."},{"key":"8267_CR44","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1038\/nrg3095","volume":"13","author":"PJ Wittkopp","year":"2012","unstructured":"Wittkopp PJ, Kalay G. Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet. 2012;13:59\u201369.","journal-title":"Nat Rev Genet"},{"key":"8267_CR45","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.tig.2016.11.003","volume":"33","author":"KL Mack","year":"2017","unstructured":"Mack KL, Nachman MW. Gene Regulation and Speciation. Trends Genet. 2017;33:68\u201380.","journal-title":"Trends Genet"},{"key":"8267_CR46","doi-asserted-by":"crossref","unstructured":"Signor SA, Nuzhdin S, v. The Evolution of Gene Expression in cis and trans. Trends Genet.\u00a02018;34:532\u201344.","DOI":"10.1016\/j.tig.2018.03.007"},{"key":"8267_CR47","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1139\/gen-2020-0025","volume":"64","author":"B Patlar","year":"2021","unstructured":"Patlar B, Civetta A. Speciation and changes in male gene expression in Drosophila. Genome. 2021;64:63\u201373.","journal-title":"Genome."},{"key":"8267_CR48","first-page":"3035","volume":"64","author":"J Lachance","year":"2010","unstructured":"Lachance J, True JR. X-autosome incompatibilities in Drosophila melanogaster: Tests of Haldane\u2019s rule and geographic patterns within species. Evolution. 2010;64:3035\u201346.","journal-title":"Evolution."},{"key":"8267_CR49","volume-title":"Rapidly Evolving Genes and Genetic Systems","author":"M Long","year":"2013","unstructured":"Long M, Vibranovski MD, Zhang YE. Evolutionary interactions between sex chromosomes and autosomes. In: Rapidly Evolving Genes and Genetic Systems; 2013."},{"key":"8267_CR50","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1534\/genetics.119.302202","volume":"212","author":"Y Bi","year":"2019","unstructured":"Bi Y, Ren X, Li R, Ding Q, Xie D, Zhao Z. Specific interactions between autosome and X chromosomes cause hybrid male sterility in Caenorhabditis species. Genetics. 2019;212:801\u201313.","journal-title":"Genetics."},{"key":"8267_CR51","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1186\/1475-4924-1-5","volume":"1","author":"PT Spellman","year":"2002","unstructured":"Spellman PT, Rubin GM. Evidence for large domains of similarly expressed genes in the Drosophila genome. J Biol. 2002;1:5.","journal-title":"J Biol"},{"key":"8267_CR52","doi-asserted-by":"publisher","first-page":"1435","DOI":"10.1093\/nar\/gki281","volume":"33","author":"AI Kalmykova","year":"2005","unstructured":"Kalmykova AI, Nurminsky DI, Ryzhov DV, Shevelyov YY. Regulated chromatin domain comprising cluster of co-expressed genes in Drosophila melanogaster. Nucleic Acids Res. 2005;33:1435\u201344.","journal-title":"Nucleic Acids Res"},{"key":"8267_CR53","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1093\/genetics\/72.1.143","volume":"72","author":"S Prakash","year":"1972","unstructured":"Prakash S. Origin of reproductive isolation in the absence of apparent genic differentiation in a geographic isolate of Drosophila pseudoobscura. Genetics. 1972;72:143\u201355.","journal-title":"Genetics."},{"key":"8267_CR54","doi-asserted-by":"publisher","first-page":"266","DOI":"10.1111\/j.1558-5646.1998.tb05161.x","volume":"52","author":"RR Snook","year":"1998","unstructured":"Snook RR. Sperm production and sterility in hybrids between two subspecies of Drosophila pseudoobscura. Evolution. 1998;52:266\u20139.","journal-title":"Evolution."},{"key":"8267_CR55","doi-asserted-by":"publisher","first-page":"1775","DOI":"10.1111\/jeb.12428","volume":"27","author":"S Gomes","year":"2014","unstructured":"Gomes S, Civetta A. Misregulation of spermatogenesis genes in Drosophila hybrids is lineage-specific and driven by the combined effects of sterility and fast male regulatory divergence. J Evol Biol. 2014;27:1775\u201383.","journal-title":"J Evol Biol"},{"key":"8267_CR56","doi-asserted-by":"publisher","first-page":"dev197558","DOI":"10.1242\/dev.197558","volume":"148","author":"JM Scovell","year":"2021","unstructured":"Scovell JM, Bournat JC, Szafran AT, Solis M, Moore J, Rivera A, et al. PRSS50 is a testis protease responsible for proper sperm tail formation and function. Development (Cambridge). 2021;148:dev197558.","journal-title":"Development (Cambridge)"},{"key":"8267_CR57","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/S0022-1910(00)00109-8","volume":"47","author":"M Friedl\u00e4nder","year":"2001","unstructured":"Friedl\u00e4nder M, Jeshtadi A, Reynolds SE. The structural mechanism of trypsin-induced intrinsic motility in Manduca sexta spermatozoa in vitro. J Insect Physiol. 2001;47:245\u201355.","journal-title":"J Insect Physiol"},{"key":"8267_CR58","doi-asserted-by":"publisher","DOI":"10.1016\/j.jinsphys.2021.104201","volume":"130","author":"JG Shepherd","year":"2021","unstructured":"Shepherd JG, Sartoris BK. Activation of parasperm and eusperm upon ejaculation in Lepidoptera. J Insect Physiol. 2021;130:104201.","journal-title":"J Insect Physiol"},{"key":"8267_CR59","doi-asserted-by":"publisher","first-page":"1542","DOI":"10.1073\/pnas.1109912109","volume":"109","author":"Y Zhao","year":"2012","unstructured":"Zhao Y, Sun W, Zhang P, Chi H, Zhang MJ, Song CQ, et al. Nematode sperm maturation triggered by protease involves sperm-secreted serine protease inhibitor (Serpin). Proc Natl Acad Sci U S A. 2012;109:1542\u20137.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"8267_CR60","doi-asserted-by":"publisher","first-page":"899","DOI":"10.1038\/aja.2010.82","volume":"12","author":"N Subir\u00e1n","year":"2010","unstructured":"Subir\u00e1n N, Pinto FM, Agirregoitia E, Candenas L, Irazusta J. Control of APN\/CD13 and NEP\/CD10 on sperm motility. Asian J Androl. 2010;12:899\u2013902.","journal-title":"Asian J Androl"},{"key":"8267_CR61","doi-asserted-by":"publisher","first-page":"1334","DOI":"10.1177\/1933719114536473","volume":"21","author":"JS Bosler","year":"2014","unstructured":"Bosler JS, Davies KP, Neal-Perry GS. Peptides in seminal fluid and their role in infertility: A potential role for opiorphin inhibition of neutral endopeptidase activity as a clinically relevant modulator of sperm motility: A review. Reprod Sci. 2014;21:1334\u201340.","journal-title":"Reprod Sci"},{"key":"8267_CR62","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1093\/molbev\/msl142","volume":"24","author":"AJ Moehring","year":"2007","unstructured":"Moehring AJ, Teeter KC, Noor MAF. Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages. Mol Biol Evol. 2007;24:137\u201345.","journal-title":"Mol Biol Evol"},{"key":"8267_CR63","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1038\/hdy.2016.31","volume":"117","author":"E Brill","year":"2016","unstructured":"Brill E, Kang L, Michalak K, Michalak P, Price DK. Hybrid sterility and evolution in Hawaiian Drosophila: Differential gene and allele-specific expression analysis of backcross males. Heredity. 2016;117:100\u20138.","journal-title":"Heredity."},{"key":"8267_CR64","doi-asserted-by":"publisher","first-page":"9844","DOI":"10.1038\/s41598-021-89366-2","volume":"11","author":"CA Banho","year":"2021","unstructured":"Banho CA, M\u00e9rel V, Oliveira TYK, Carareto CMA, Vieira C. Comparative transcriptomics between Drosophila mojavensis and D. arizonae reveals transgressive gene expression and underexpression of spermatogenesis-related genes in hybrid testes. Sci Rep. 2021;11:9844.","journal-title":"Sci Rep"},{"key":"8267_CR65","doi-asserted-by":"publisher","first-page":"1098","DOI":"10.1126\/science.1062939","volume":"293","author":"S Henikoff","year":"2001","unstructured":"Henikoff S, Ahmad K, Malik HS. The centromere paradox: Stable inheritance with rapidly evolving DNA. Science. 2001;293:1098\u2013102.","journal-title":"Science."},{"key":"8267_CR66","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1038\/417227a","volume":"417","author":"S Henikoff","year":"2002","unstructured":"Henikoff S. Malik HS. Centromeres: Selfish drivers. Nature. 2002;417:227.","journal-title":"Nature."},{"key":"8267_CR67","doi-asserted-by":"publisher","first-page":"4309","DOI":"10.3390\/ijms22094309","volume":"22","author":"J Thakur","year":"2021","unstructured":"Thakur J, Packiaraj J, Henikoff S. Sequence, chromatin and evolution of satellite DNA. Int J Mol Sci. 2021;22:4309.","journal-title":"Int J Mol Sci"},{"key":"8267_CR68","doi-asserted-by":"publisher","first-page":"1538","DOI":"10.1126\/science.1181756","volume":"326","author":"JJ Bayes","year":"2009","unstructured":"Bayes JJ, Malik HS. Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science. 2009;326:1538\u201341.","journal-title":"Science."},{"key":"8267_CR69","doi-asserted-by":"publisher","first-page":"1559","DOI":"10.1126\/science.1161406","volume":"322","author":"L Fishman","year":"2008","unstructured":"Fishman L, Saunders A. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science. 2008;322:1559\u201362.","journal-title":"Science."},{"key":"8267_CR70","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1111\/evo.12661","volume":"69","author":"L Fishman","year":"2015","unstructured":"Fishman L, Kelly JK. Centromere-associated meiotic drive and female fitness variation in Mimulus. Evolution. 2015;69:1208\u201318.","journal-title":"Evolution."},{"key":"8267_CR71","doi-asserted-by":"publisher","first-page":"4702","DOI":"10.1016\/j.jmb.2018.08.007","volume":"430","author":"G Seydoux","year":"2018","unstructured":"Seydoux G, The P. Granules of C. elegans: A Genetic Model for the Study of RNA\u2013Protein Condensates. J Mol Biol. 2018;430:4702\u201310.","journal-title":"J Mol Biol"},{"key":"8267_CR72","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.devcel.2019.11.007","volume":"52","author":"V Bhargava","year":"2020","unstructured":"Bhargava V, Goldstein CD, Russell L, Xu L, Ahmed M, Li W, et al. GCNA Preserves Genome Integrity and Fertility Across Species. Dev Cell. 2020;52:38\u201352.","journal-title":"Dev Cell"},{"key":"8267_CR73","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.21491","volume":"5","author":"J Lopez-Mosqueda","year":"2016","unstructured":"Lopez-Mosqueda J, Maddi K, Prgomet S, Kalayil S, Marinovic-Terzic I, Terzic J, et al. SPRTN is a mammalian DNA-binding metalloprotease that resolves DNA-protein crosslinks. eLife. 2016;5:e21491.","journal-title":"eLife."},{"key":"8267_CR74","doi-asserted-by":"publisher","first-page":"704","DOI":"10.1016\/j.molcel.2016.09.032","volume":"64","author":"B Vaz","year":"2016","unstructured":"Vaz B, Popovic M, Newman JA, Fielden J, Aitkenhead H, Halder S, et al. Metalloprotease SPRTN\/DVC1 Orchestrates Replication-Coupled DNA-Protein Crosslink Repair. Mol Cell. 2016;64:704\u201319.","journal-title":"Mol Cell"},{"key":"8267_CR75","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1038\/nrm.2017.56","volume":"18","author":"J Stingele","year":"2017","unstructured":"Stingele J, Bellelli R, Boulton SJ. Mechanisms of DNA-protein crosslink repair. Nat Rev Mol Cell Biol. 2017;18:563\u201373.","journal-title":"Nat Rev Mol Cell Biol"},{"key":"8267_CR76","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1038\/ng.77","volume":"40","author":"PJ Wittkopp","year":"2008","unstructured":"Wittkopp PJ, Haerum BK, Clark AG. Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet. 2008;40:346\u201350.","journal-title":"Nat Genet"},{"key":"8267_CR77","doi-asserted-by":"publisher","first-page":"816","DOI":"10.1101\/gr.102491.109","volume":"20","author":"CJ McManus","year":"2010","unstructured":"McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, Wittkopp PJ. Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res. 2010;20:816\u201325.","journal-title":"Genome Res"},{"key":"8267_CR78","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1101\/gr.195743.115","volume":"26","author":"KL Mack","year":"2016","unstructured":"Mack KL, Campbell P, Nachman MW. Gene regulation and speciation in house mice. Genome Res. 2016;26:451\u201361.","journal-title":"Genome Res"},{"key":"8267_CR79","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1009409","volume":"17","author":"S S\u00e1nchez-Ram\u00edrez","year":"2021","unstructured":"S\u00e1nchez-Ram\u00edrez S, Weiss JG, Thomas CG, Cutter AD. Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution. PLoS Genet. 2021;17:e1009409.","journal-title":"PLoS Genet"},{"key":"8267_CR80","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1038\/s41576-020-00304-w","volume":"22","author":"MS Hill","year":"2021","unstructured":"Hill MS, vande Zande P, Wittkopp PJ. Molecular and evolutionary processes generating variation in gene expression. Nat Rev Genet. 2021;22:203\u201315.","journal-title":"Nat Rev Genet"},{"key":"8267_CR81","doi-asserted-by":"publisher","first-page":"1331","DOI":"10.1093\/genetics\/144.4.1331","volume":"144","author":"HA Orr","year":"1996","unstructured":"Orr HA. Dobzhansky, Bateson, and the genetics of speciation. Genetics. 1996;144:1331\u20135.","journal-title":"Genetics."},{"key":"8267_CR82","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1080\/19336934.2020.1864201","volume":"15","author":"KL Korunes","year":"2021","unstructured":"Korunes KL, Myers RB, Hardy R, Noor MAF. PseudoBase: a genomic visualization and exploration resource for the Drosophila pseudoobscura subgroup. Fly. 2021;15:38\u201344.","journal-title":"Fly."},{"key":"8267_CR83","doi-asserted-by":"publisher","first-page":"3022","DOI":"10.1093\/molbev\/msab120","volume":"38","author":"K Tamura","year":"2021","unstructured":"Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol. 2021;38:3022\u20137.","journal-title":"Mol Biol Evol"},{"key":"8267_CR84","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1111\/j.1558-5646.1985.tb00420.x","volume":"39","author":"J Felsenstein","year":"1985","unstructured":"Felsenstein J. Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution. 1985;39:783\u201391.","journal-title":"Evolution."},{"key":"8267_CR85","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1038\/nmeth0410-248","volume":"7","author":"IA Adzhubei","year":"2010","unstructured":"Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010;7:248\u20139.","journal-title":"Nat Methods"},{"key":"8267_CR86","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0046688","volume":"7","author":"Y Choi","year":"2012","unstructured":"Choi Y, Sims GE, Murphy S, Miller JR, Chan AP. Predicting the Functional Effect of Amino Acid Substitutions and Indels. PLoS One. 2012;7:e46688.","journal-title":"PLoS One"},{"key":"8267_CR87","volume-title":"FastQC - A quality control tool for high throughput sequence data","author":"S Andrews","year":"2010","unstructured":"Andrews S. FastQC - A quality control tool for high throughput sequence datahttp:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/. Babraham Bioinformatics; 2010."},{"key":"8267_CR88","doi-asserted-by":"publisher","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","volume":"30","author":"AM Bolger","year":"2014","unstructured":"Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114\u201320.","journal-title":"Bioinformatics."},{"key":"8267_CR89","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","volume":"29","author":"A Dobin","year":"2013","unstructured":"Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15\u201321.","journal-title":"Bioinformatics."},{"key":"8267_CR90","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1093\/bioinformatics\/btt656","volume":"30","author":"Y Liao","year":"2014","unstructured":"Liao Y, Smyth GK, Shi W. FeatureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923\u201330.","journal-title":"Bioinformatics."},{"key":"8267_CR91","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.","journal-title":"Genome Biol"},{"key":"8267_CR92","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","volume":"26","author":"D Robinson Mark","year":"2010","unstructured":"Robinson Mark D, McCarthy Davis J, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139\u201340.","journal-title":"Bioinformatics."},{"key":"8267_CR93","first-page":"1438","volume":"5","author":"Y Chen","year":"2016","unstructured":"Chen Y, Lun ATL, Smyth GK. From reads to genes to pathways: Differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Research. 2016;5:1438.","journal-title":"F1000Research"},{"key":"8267_CR94","doi-asserted-by":"publisher","first-page":"R25","DOI":"10.1186\/gb-2010-11-3-r25","volume":"11","author":"MD Robinson","year":"2010","unstructured":"Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11:R25.","journal-title":"Genome Biol"},{"key":"8267_CR95","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1261\/rna.053959.115","volume":"22","author":"NJ Schurch","year":"2016","unstructured":"Schurch NJ, Schofield P, Gierli\u0144ski M, Cole C, Sherstnev A, Singh V, et al. How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? RNA. 2016;22:839\u201351.","journal-title":"RNA."},{"key":"8267_CR96","doi-asserted-by":"publisher","first-page":"3299","DOI":"10.1093\/molbev\/msx248","volume":"34","author":"J Rozas","year":"2017","unstructured":"Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299\u2013302.","journal-title":"Mol Biol Evol"},{"key":"8267_CR97","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1093\/bioinformatics\/18.2.333","volume":"18","author":"X Messeguer","year":"2002","unstructured":"Messeguer X, Escudero R, Farr\u00e9 D, N\u00fa\u00f1ez O, Mart\u00ednez J, Alb\u00e0 MM. PROMO: Detection of known transcription regulatory elements using species-tailored searches. Bioinformatics. 2002;18:333\u20134.","journal-title":"Bioinformatics."},{"key":"8267_CR98","doi-asserted-by":"publisher","first-page":"3651","DOI":"10.1093\/nar\/gkg605","volume":"31","author":"D Farr\u00e9","year":"2003","unstructured":"Farr\u00e9 D, Roset R, Huerta M, Adsuara JE, Rosell\u00f3 L, Alb\u00e0 MM, et al. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res. 2003;31:3651\u20133.","journal-title":"Nucleic Acids Res"},{"key":"8267_CR99","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1186\/gb4161","volume":"15","author":"D Blankenberg","year":"2014","unstructured":"Blankenberg D, von Kuster G, Bouvier E, Baker D, Afgan E, Stoler N, et al. Dissemination of scientific software with Galaxy ToolShed. Genome Biol. 2014;15:403.","journal-title":"Genome Biol"}],"container-title":["BMC Genomics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-021-08267-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12864-021-08267-w\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12864-021-08267-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,23]],"date-time":"2022-10-23T00:04:34Z","timestamp":1666483474000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcgenomics.biomedcentral.com\/articles\/10.1186\/s12864-021-08267-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,6]]},"references-count":99,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["8267"],"URL":"https:\/\/doi.org\/10.1186\/s12864-021-08267-w","relation":{},"ISSN":["1471-2164"],"issn-type":[{"value":"1471-2164","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,6]]},"assertion":[{"value":"13 August 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 December 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 January 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"30"}}