Cis-regulatory divergence and misexpression of spermatogenesis genes underlie hybrid male sterility in the species complex

Adobe Systems Inc. (2022) Adobe illustrator. Version 26.0. San Jose, CA: Adobe Systems

Assis R, Zhou Q, Bachtrog D (2012) Sex-biased transcriptome evolution in Drosophila. Genome Biol Evol 4(11):1189–1200. https://doi.org/10.1093/gbe/evs093

Article  CAS  PubMed  PubMed Central  Google Scholar 

Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43(W1):W39-49. https://doi.org/10.1093/nar/gkv416

Article  CAS  PubMed  PubMed Central  Google Scholar 

Barbash DA, Lorigan JG (2007) Lethality and sterility in Drosophila hybrids: two sides of the same coin? Genetica 129(1):97–108. https://doi.org/10.1007/s10709-006-9017-5

Article  Google Scholar 

Castro-Mondragon JA, Riudavets-Puig R, Rauluseviciute I, Berhanu Lemma R, Turchi L, Blanc-Mathieu R et al (2022) JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res 50(D1):D165–D173. https://doi.org/10.1093/nar/gkab1113

Article  CAS  PubMed  PubMed Central  Google Scholar 

Catron DJ, Noor MAF (2008) Gene expression disruptions in hybrids of Drosophila pseudoobscura and D. persimilis. PLoS ONE 3(12):e3006. https://doi.org/10.1371/journal.pone.0003006

Article  CAS  Google Scholar 

Civetta A (2016) Misregulation of gene expression and sterility in interspecies hybrids: causal links and alternative hypotheses. J Mol Evol 82(4–5):176–182. https://doi.org/10.1007/s00239-016-9732-8

Article  CAS  PubMed  Google Scholar 

Civetta A, Singh RS (1995) High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol 41(6):1085–1095. https://doi.org/10.1007/BF00173162

Article  CAS  PubMed  Google Scholar 

Coulthart MB, Singh RS (1988) High level of divergence of male reproductive tract proteins between sibling species of the Drosophila melanogaster subgroup. Mol Biol Evol 5(2):182–191. https://doi.org/10.1093/oxfordjournals.molbev.a040485

Article  CAS  PubMed  Google Scholar 

Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

Google Scholar 

Dobzhansky T (1934) Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura. Genetics 19(2):130–155. https://doi.org/10.1093/genetics/19.2.130

Article  Google Scholar 

Ferguson KA, Mohajeri P, Civetta A (2013) Gene expression changes following hybridization are widespread and affect spermatogenesis genes. J Evol Biol 26(6):1183–1193. https://doi.org/10.1111/jeb.12127

Article  Google Scholar 

FlyBase Consortium (2003) The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res 31(1):172–175. https://doi.org/10.1093/nar/gkg094

Article  CAS  Google Scholar 

Fuller MT (1993) Spermatogenesis. In: Bate M, Martinez-Arias A (eds) The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 71–147

Google Scholar 

Fuller MT (1998) CREM: a master–switch governing male germ cells differentiation and apoptosis. Semin Cell Dev Biol 9(4):433–444. https://doi.org/10.1006/scdb.1998.0200

Article  CAS  PubMed  Google Scholar 

Gomes S, Civetta A (2014) A Drosophila laboratory evolution experiment points to low evolutionary potential under increased temperatures likely to be experienced in the future. J Evol Biol 27(9):1779–1788. https://doi.org/10.1111/jeb.12436

Article  Google Scholar 

Grant CE, Bailey TL, Noble WS (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27(7):1017–1018. https://doi.org/10.1093/bioinformatics/btr064

Article  CAS  PubMed  PubMed Central  Google Scholar 

GraphPad Software (2021) GraphPad Prism. Version 9. San Diego, CA: GraphPad Software. Available from: https://www.graphpad.com

Grath S, Parsch J (2012) Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46(1):51–72. https://doi.org/10.1146/annurev-genet-110711-155529

Article  CAS  Google Scholar 

Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, Sirot LK et al (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177(3):1321–1335. https://doi.org/10.1534/genetics.107.078865

Article  CAS  PubMed  PubMed Central  Google Scholar 

Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12(2):101–109. https://doi.org/10.1007/BF02983075

Article  Google Scholar 

Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9(9):868–877. https://doi.org/10.1101/gr.9.9.868

Article  CAS  PubMed  PubMed Central  Google Scholar 

Hunter JD (2007) Matplotlib: a 2D graphics environment. Comput Sci Eng 9(3):90–95. https://doi.org/10.1109/MCSE.2007.55

Article  Google Scholar 

Jiang J, White-Cooper H (2003) Transcriptional activation in Drosophila spermatogenesis involves the mutually dependent function of aly and comr, two meiotic arrest genes. Development 130(20):563–573. https://doi.org/10.1242/dev.00752

Article  CAS  PubMed  Google Scholar 

Kulathinal RJ, Singh RS (1998) Cytological characterization of premeiotic versus postmeiotic defects producing hybrid male sterility among sibling species of the Drosophila melanogaster complex. Evolution 52(3):625–636. https://doi.org/10.1111/j.1558-5646.1998.tb03682.x

Article  Google Scholar 

Lachaise D, Cariou ML, David JR, Lemeunier F, Tsacas L, Ashburner M (1986) Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol 20:159–225. https://doi.org/10.1007/978-1-4615-6982-5_5

Article  Google Scholar 

Landry CR, Hartl DL, Ranz JM (2007) Genome clashes in hybrids: insights from gene expression. Heredity 99(5):483–493. https://doi.org/10.1038/sj.hdy.6801045

Article  CAS  PubMed  Google Scholar 

Liénard MA, Oudin MJ, Culi J, Loppin B (2016) Specific targeting of a duplicated gene family by a transposable element drives hybrid male sterility in Drosophila. Proc Natl Acad Sci USA 113(15):E2262–E2271. https://doi.org/10.1073/pnas.1522252113

Article  Google Scholar 

Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45(1):331–355. https://doi.org/10.1146/annurev-genet-110410-132514

Article  CAS  PubMed  Google Scholar 

Malone JH, Michalak P, Noor MAF (2007) Sterility and gene expression in interspecific hybrids of Xenopus. Evolution 61(2):275–283. https://doi.org/10.1111/j.1558-5646.2007.00027.x

Article  Google Scholar 

Manjunath M, Shakunthala V (2023) Diversifying selection in aly, bam, dj and topi genes: association between rapid divergence and hybrid male sterility in Drosophila bipectinata species complex. Gene Rep 33:101836. https://doi.org/10.1016/j.genrep.2023.101836

Article  CAS  Google Scholar 

Masly JP, Presgraves DC (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5(9):e243. https://doi.org/10.1371/journal.pbio.0050243

Article  CAS  PubMed  PubMed Central  Google Scholar 

Meiklejohn CD, Parsch J, Ranz JM, Hartl DL (2003) Rapid evolution of male-biased gene expression in Drosophila. Nature 421(6925):712–715. https://doi.org/10.1038/nature01304

Article  CAS  Google Scholar 

Michalak P, Ma D (2008) Loss of heterozygosity and expression changes in hybrids: a case study of Drosophila. BMC Genomics 9:424. https://doi.org/10.1186/1471-2164-9-424

Article  CAS  Google Scholar 

Michalak P, Noor MAF (2003) Genome-wide patterns of expression in Drosophila pure species and hybrids. Evolution 57(3):755–759. https://doi.org/10.1111/j.0014-3820.2003.tb00288.x

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