Abstract
The crosses between closely related Drosophila species usually produce sterile hybrid males with spermatogenesis disrupted at post-meiotic phase, especially in sperm individualization stage than the pre-meiotic stage. This is possibly due to the rapid interspecies divergence of male sex and reproduction-related genes. Here we annotated 11 key spermatogenesis genes in 35 strains of species belonging to nasuta-subgroup of Drosophila, where many interspecies crosses produce sterile males. We characterized the divergence and polymorphism in the protein coding regions by employing gene-wide, codon-wide, and lineage-specific selection analysis to test the mode and strength of selection acting on these genes. Our analysis showed signature of positive selection at bag of marbles (bam) and benign gonial cell neoplasma (bgcn) despite the selection constrains and the absence of endosymbiont infection which could potentially drive rapid divergence due to an arms race while roughex (rux) showed lineage-specific rapid divergence in frontal sheen complex of nasuta-subgroup. cookie monster (comr) showed rapid divergence consistent with the possibility of meiotic arrest observed in sterile hybrids of Drosophila species. Rapid divergence observed at don juan (dj) and Mst98Ca-like was consistent with fused sperm-tail abnormality observed in the hybrids of Drosophila nasuta and Drosophila albomicans. These findings highlight the potential role of rapid nucleotide divergence in bringing about hybrid incompatibility in the form of male sterility; however, additional genetic manipulation studies can widen our understanding of hybrid incompatibilities. Furthermore, our study emphasizes the importance of young species belonging to nasuta-subgroup of Drosophila in studying post-zygotic reproductive isolation mechanisms.
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References
Avedisov SN, Rogozin IB, Koonin EV, Thomas BJ (2001) Rapid evolution of a cyclin A inhibitor gene, roughex, in Drosophila. Mol Biol Evol 18:2110–2118. https://doi.org/10.1093/oxfordjournals.molbev.a003752
Ayyar S, Jiang J, Collu A, White-Cooper H, White RAH (2003) Drosophila TGIF is essential for developmentally regulated transcription in spermatogenesis. Development 130:2841–2852. https://doi.org/10.1242/dev.00513
Bateson W (1909) Heredity and variation in modern lights. In: Darwin and Modern Science. Cambridge University Press, Cambridge, pp. 85–101
Bauer DuMont VL, Flores HA, Wright MH, Aquadro CF (2007a) Recurrent positive selection at Bgcn, a key determinant of germ line differentiation, does not appear to be driven by simple coevolution with its partner protein bam. Mol Biol Evol 24:182–191. https://doi.org/10.1093/molbev/msl141
Bayes JJ, Malik HS (2009) Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326:1538–1541. https://doi.org/10.1126/science.1181756
Beitel GJ, Lambie EJ, Horvitz HR (2000) The C. elegans gene lin-9, which acts in an Rb-related pathway, is required for gonadal sheath cell development and encodes a novel protein. Gene 254:253–263. https://doi.org/10.1016/S0378-1119(00)00296-1
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300
Blanco G, Mercer RW (1998) Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol Ren Physiol. https://doi.org/10.1152/ajprenal.1998.275.5.f633
Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314:1292–1295. https://doi.org/10.1126/science.1133953
Catron DJ, Noor MAF (2008) Gene expression disruptions of organism versus organ in Drosophila Species hybrids. PLoS ONE 3:e3009. https://doi.org/10.1371/journal.pone.0003009
Choi JY, Aquadro CF (2014) The coevolutionary period of Wolbachia pipientis infecting Drosophila ananassae and its impact on the evolution of the host germline stem cell regulating genes. Mol Biol Evol 31:2457–2471. https://doi.org/10.1093/molbev/msu204
Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet 9:1003896. https://doi.org/10.1371/journal.pgen.1003896
Civetta A, Rajakumar SA, Brouwers B, Bacik JP (2006) Rapid evolution and gene-specific patterns of selection for three genes of spermatogenesis in Drosophila. Mol Biol Evol 23:655–662. https://doi.org/10.1093/molbev/msj074
Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381. https://doi.org/10.1111/j.1558-5646.1989.tb04233.x
Coyne JA, Orr HA (1997) “Patterns of speciation in Drosophila” revisited. Evolution 51:295
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Inc.
Cutter AD, Ward S (2005) Sexual and temporal dynamics of molecular evolution in C. elegans development. Mol Biol Evol 22:178–188. https://doi.org/10.1093/molbev/msh267
Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York
Doggett K, Jiang J, Aleti G, White-Cooper H (2011) Wake-up-call, a lin-52 paralogue, and always early, a lin-9 homologue physically interact, but have opposing functions in regulating testis-specific gene expression. Dev Biol 355:381–393. https://doi.org/10.1016/j.ydbio.2011.04.030
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A, Sonnhammer ELL, Hirsh L, Paladin L, Piovesan D, Tosatto SCE, Finn RD (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432. https://doi.org/10.1093/nar/gky995
Ellegren H, Parsch J (2007) The evolution of sex-biased genes and sex-biased gene expression. Nat Rev Genet. https://doi.org/10.1038/nrg2167
Flores HA, Bubnell JE, Aquadro CF, Barbash DA (2015) The Drosophila bag of marbles gene interacts genetically with Wolbachia and shows female-specific effects of divergence. PLoS Genet 11(8):e1005453. https://doi.org/10.1371/journal.pgen.1005453
Frank SA (1991) Divergence of meiotic drive-suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45:262–267. https://doi.org/10.1111/j.1558-5646.1991.tb04401.x
Fuller MT (1998) Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin Cell Dev Biol 9:433–444. https://doi.org/10.1006/scdb.1998.0227
Gerts EM, Yu YK, Agarwala R, Schäffer AA, Altschul SF (2006) Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol 4:41. https://doi.org/10.1186/1741-7007-4-41
Gigliotti S, Balz V, Malva C, Schäfer MA (1997) Organisation of regulatory elements in two closely spaced Drosophila genes with common expression characteristics. Mech Dev 68:101–113. https://doi.org/10.1016/S0925-4773(97)00137-8
Gouy M, Guindon S, Gascuel O (2010) Sea view version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. https://doi.org/10.1093/molbev/msp259
Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ram KR, Sirot LK, Levesque L, Artieri CG, Wolfner MF, Civetta A, Singh RS (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177:1321–1335. https://doi.org/10.1534/genetics.107.078865
Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101–109. https://doi.org/10.1007/BF02983075
Hartl DL (1975) Modifier theory and meiotic drive. Theor Popul Biol 7:168–174. https://doi.org/10.1016/0040-5809(75)90012-X
Hatsumi M, Morishige Y, Wakahama KI (1988) Metaphase chromosomes of four species of the Drosophila nasuta subgroup. Jpn J Genet 63:435–444. https://doi.org/10.1266/jjg.63.435
Hiller MA, Lin TY, Wood C, Fuller MT (2001) Developmental regulation of transcription by a tissue-specific TAF homolog. Genes Dev 15:1021–1030. https://doi.org/10.1101/gad.869101
Hiller M, Chen X, Pringle MJ, Suchorolski M, Sancak Y, Viswanathan S, Bolival B, Lin TY, Marino S, Fuller MT (2004) Testis-specific TAF homologs collaborate to control a tissue-specific transcription program. Development 131:5297–5308. https://doi.org/10.1242/dev.01314
Hoekstra HE, Coyne JA (2007) The locus of evolution: evo devo and the genetics of adaptation. Evolution. https://doi.org/10.1111/j.1558-5646.2007.00105.x
Hurst LD, Pomiankowski A (1991) Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane’s rule and related phenomena. Genetics 128:841–858
Ito T (2001) Novel modular domain PB1 recognizes PC motif to mediate functional protein-protein interactions. EMBO J 20:3938–3946. https://doi.org/10.1093/emboj/20.15.3938
Jiang J, White-Cooper H (2003) Transcriptional activation in Drosophila spermatogenesis involves the mutually dependent function of aly and a novel meiotic arrest gene cookie monster. Development. https://doi.org/10.1242/dev.00246
Kitagawa O, Wakahama K-I, Fuyama Y, Shimada Y, Takanashi E, Hatsumi M, Uwabo M, Mita Y (1982) Genetic studies of the Drosophila nasuta subgroup, with notes on distribution and morphology. Jpn J Genet 57:113
Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679. https://doi.org/10.1093/bioinformatics/bti079
Kosakovsky Pond SL, Murrell B, Fourment M, Frost SDW, Delport W, Scheffler K (2011) A random effects branch-site model for detecting episodic diversifying selection. Mol Biol Evol 28:3033–3043. https://doi.org/10.1093/molbev/msr125
Kuhn R, Schäfer U, Schäfer M (1988) Cis-acting regions sufficient for spermatocyte-specific transcriptional and spermatid-specific translational control of the Drosophila melanogaster gene mst(3)gl-9. EMBO J 7:447–454. https://doi.org/10.1002/j.1460-2075.1988.tb02832.x
Kulathinal R, Singh RS (1998) Cytological characterization of premeiotic versus postmeiotic defects producing hybrid male sterility among sibling species of the Drosophila melanogaster complex. Evolution 52:1067–1079. https://doi.org/10.1111/j.1558-5646.1998.tb01834.x
Lachaise D, David JR, Lemeunier F, Tsacas L, Ashburner M (1986) The reproductive relationships of drosophila sechellia with d. mauritiana, D. simulans, and D. melanogaster from the afrotropical region. Evolution 40:262–271. https://doi.org/10.1111/j.1558-5646.1986.tb00468.x
Lavoie CA, Ohlstein B, McKearin DM (1999) Localization and function of bam protein require the benign gonial cell neoplasm gene product. Dev Biol 212:405–413. https://doi.org/10.1006/dbio.1999.9346
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lifschytz E, Meyer GF (1977) Characterisation of male meiotic-sterile mutations in Drosophila melanogaster—the genetic control of meiotic divisions and gametogenesis. Chromosoma 64:371–392. https://doi.org/10.1007/BF00294944
Llopart A, Comeron JM (2008) Recurrent events of positive selection in independent Drosophila lineages at the spermatogenesis gene roughex. Genetics 179:1009–1020. https://doi.org/10.1534/genetics.107.086231
Mai D, Nalley MJ, Bachtrog D (2020) Patterns of genomic differentiation in the Drosophila nasuta Species complex. Mol Biol Evol 37:208–220. https://doi.org/10.1093/molbev/msz215
Marygold SJ, Leyland PC, Seal RL, Goodman JL, Strelets VB, Wilson RJ, Ashburner M, Drysdale R, de Grey A, Gelbart W, Broll K, Crosby L, dos Santos G, Emmert D, Falls K, Gramates LS, Matthews B, Russo S, Schroeder A, StPierre S, Zhou P, Zytkovicz M, Brown NH, Adryan B, Attrill H, Costa M, Field H, Marigold S, McQuilton P, Millburn G, Ponting L, Osumi-Sutherland D, Stefancsik R, Tweedie S, Kaufman T, Matthews K, Goodmen J, Grumbling G, Strelts V, Thurmond J, Wong JD, Werner-Washburne M, Cripps R, Platero H (2013) FlyBase: Improvements to the bibliography. Nucleic Acids Res 41:D751–D757. https://doi.org/10.1093/nar/gks1024
Masly JP, Presgraves DC (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5:e243. https://doi.org/10.1371/journal.pbio.0050243
Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA (2006) Heritable endosymbionts of Drosophila. Genetics 174:363–376. https://doi.org/10.1534/genetics.106.058818
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654
McKearin D, Ohlstein B (1995) A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 121:2937
Meiklejohn CD, Tao Y (2010) Genetic conflict and sex chromosome evolution. Trends Ecol Evol 25:215–223. https://doi.org/10.1016/j.tree.2009.10.005
Michalak P, Noor MAF (2003) Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol Biol Evol 20:1070–1076. https://doi.org/10.1093/molbev/msg119
Michalak P, Noor MAF (2004) Association of misexpression with sterility in hybrids of Drosophila simulans and D. mauritiana. J Mol Evol 59:277–282. https://doi.org/10.1007/s00239-004-2622-y
Moehring AJ, Teeter KC, Noor MAF (2007) 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 24:137–145. https://doi.org/10.1093/molbev/msl142
Mohanty S, Khanna R (2017) Genome-wide comparative analysis of four Indian Drosophila species. Mol Genet Genomics 292:1197–1208. https://doi.org/10.1007/s00438-017-1339-8
Morohashi K, Sahara H, Watashi K, Iwabata K, Sunoki T, Kuramochi K, Takakusagi K, Miyashita H, Sato N, Tanabe A, Shimotohno K, Kobayashi S, Sakaguchi K, Sugawara F (2011) Cyclosporin A associated helicase-like protein facilitates the association of hepatitis C virus RNA polymerase with its cellular cyclophilin B. PLoS ONE 6:e18285. https://doi.org/10.1371/journal.pone.0018285
Muller H (1942) Isolating mechanisms, evolution and temperature. Biol Symp 71–125
Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:1002764. https://doi.org/10.1371/journal.pgen.1002764
Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained bayesian AppRoximation for inferring selection. Mol Biol Evol 30:1196–1205. https://doi.org/10.1093/molbev/mst030
Murrell B, Weaver S, Smith MD, Wertheim JO, Murrell S, Aylward A, Eren K, Pollner T, Martin DP, Smith DM, Scheffler K, Kosakovsky Pond SL (2015) Gene-wide identification of episodic selection. Mol Biol Evol 32:1365–1371. https://doi.org/10.1093/molbev/msv035
Nirmala SS, Krishnamurthy NB (1973) Cytogenetic studies on Drosophila neonasuta-A member of the nasuta subgroup. J Mysore Univ 26:162–167
Orr HA (1993) Haldane’s rule has multiple genetic causes. Nature 361:532–533. https://doi.org/10.1038/361532a0
Ortiz-Barrientos D, Chang AS, Noor MAF (2006) A recombinational portrait of the Drosophila pseudoobscura genome. Genet Res 87:23–31. https://doi.org/10.1017/S0016672306007932
Perezgasga L, Jiang JQ, Bolival B, Hiller M, Benson E, Fuller MT, White-Cooper H (2004) Regulation of transcription of meiotic cell cycle and terminal differentiation genes by the testis-specific Zn-finger protein matotopetli. Development 131:1691–1702. https://doi.org/10.1242/dev.01032
Phadnis N, Orr HA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323:376–379. https://doi.org/10.1126/science.1163934
Ponting CP, Ito T, Moscat J, Diaz-Meco MT, Inagaki F, Sumimoto H (2002) OPR, PC and AID: all in the PB1 family. Trends Biochem Sci. https://doi.org/10.1016/S0968-0004(01)02006-0
Presgraves DC (2003) A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163:955–972
Rambaut A (2010) FigTree v1.3.1. institute of evolutionary biology. University of Edinburgh, Edinburgh
Ranz JM, Machado CA (2006) Uncovering evolutionary patterns of gene expression using microarrays. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2005.09.002
Ravikumar H, Prakash BM, Sampathkumar S, Puttaraju HP (2011) Molecular subgrouping of Wolbachia and bacteriophage WO infection among some Indian Drosophila species. J Genet 90:507
Rogers S, Wells R, Rechsteiner M (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234:364–368. https://doi.org/10.1126/science.2876518
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Santel A, Winhauer T, Blümer N, Renkawitz-Pohl R (1997) The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech Dev 64:19–30. https://doi.org/10.1016/S0925-4773(97)00031-2
Santel A, Blümer N, Kämpfer M, Renkawitz-Pohl R (1998) Flagellar mitochondrial association of the male-specific Don Juan protein in Drosophila spermatozoa. J Cell Sci 111:3299–3309
Schafer M, Kuhn R, Bosse F, Schafer U (1990) A conserved element in the leader mediates post-meiotic translation as well as cytoplasmic polyadenylation of a Drosophila spermatocyte mRNA. EMBO J 9:4519–4525. https://doi.org/10.1002/j.1460-2075.1990.tb07903.x
Schulz C, Kiger AA, Tazuke SI, Yamashita YM, Pantalena-Filho LC, Jones DL, Wood CG, Fuller MT (2004) A misexpression screen reveals effects of bag-of-marbles and TGFβ class signaling on the Drosophila male germ-line stem cell lineage. Genetics 167:707–723. https://doi.org/10.1534/genetics.103.023184
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. https://doi.org/10.1038/msb.2011.75
Spieth TH (1969) Courtship and mating behavior of the Drosophila nasuta subgroup of species. Univ Tex Publ 6918:255–270
Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. https://doi.org/10.1093/nar/gki458
Stoilov P, Rafalska I, Stamm S (2002) YTH: a new domain in nuclear proteins. Trends Biochem Sci. https://doi.org/10.1016/S0968-0004(02)02189-8
Suzuki YM, Kitagawa O, Wakahama KI (1990) Chromosomal analysis and phylogenetic relationships in the Drosophila nasuta subgroup I. Phylogenetic relationships within the Drosophila sulfurigaster species complex. Genetica 80:53–66. https://doi.org/10.1007/BF00120120
Szakmary A, Cox DN, Wang Z, Lin H (2005) Regulatory relationship among piwi, pumilio, and bag-of-marbles in Drosophila germline stem cell self-renewal and differentiation. Curr Biol 15:171–178. https://doi.org/10.1016/j.cub.2005.01.005
Tao Y, Hartl DL (2003) Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. Iii. Heterogeneous accumulation of hybrid incompatibilities, degree of dominance, and implications for haldane’s rule. Evolution 57:2580. https://doi.org/10.1554/03-094
Tao Y, Chen S, Hartl DL, Laurie CC (2003) Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics 164:1383–1397
Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:W232–W235. https://doi.org/10.1093/nar/gkw256
Wakimoto BT, Lindsley DL, Herrera C (2004) Toward a comprehensive genetic analysis of male fertility in Drosophila melanogaster. Genetics 167:207–216. https://doi.org/10.1534/genetics.167.1.207
Wang Z, Mann RS (2003) Requirement for two nearly identical TGIF-related homeobox genes in Drosophila spermatogenesis. Development 130:2853–2865. https://doi.org/10.1242/dev.00510
Watts T, Haselkorn TS, Moran NA, Markow TA (2009) Variable incidence of spiroplasma infections in natural populations of Drosophila species. PLoS ONE 4:e5703. https://doi.org/10.1371/journal.pone.0005703
White MA, Stubbings M, Dumont BL, Payseur BA (2012) Genetics and evolution of hybrid male sterility in house mice. Genetics 191:917–934. https://doi.org/10.1534/genetics.112.140251
White-Cooper H, Schafer MA, Alphey LS, Fuller MT (1998) Transcriptional and post-transcriptional control mechanisms coordinate the onset of spermatid differentiation with meiosis I in Drosophila. Development 125:125–134
White-Cooper H, Leroy D, MacQueen A, Fuller MT (2000) Transcription of meiotic cell cycle and terminal differentiation genes depends on a conserved chromatin associated protein, whose nuclear localisation is regulated. Development 127(24):5463–5473
White-Cooper H (2010) Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction. https://doi.org/10.1530/REP-09-0083
White-Cooper H, Bausek N (2010) Evolution and spermatogenesis. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2009.0323
Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13:e1005595. https://doi.org/10.1371/journal.pcbi.1005595
Wilson DF (1969) Cytogenetic relations in the Drosophila nasuta subgroup of the immigrans group of species. Univ Texas Publ 6918:207–253
Woo AL, James PF, Lingrel JB (2000) Sperm motility is dependent on a unique isoform of the Na, K-ATPase. J Biol Chem 275:20693–20699. https://doi.org/10.1074/jbc.M002323200
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. https://doi.org/10.1093/molbev/msm088
Yang Y-Y, Lin F-J, Chang H (2004) Sex ratio distortion in hybrids of Drosophila albomicans and D. nasuta. Zool Stud Taipei 43:622
Yu H, Wang W, Fang S, Zhang YP, Lin FJ, Geng ZC (1999) Phylogeny and evolution of the Drosophila nasuta subgroup based on mitochondrial ND4 and ND4L gene sequences. Mol Phylogenet Evol 13(3):556–565. https://doi.org/10.1006/mpev.1999.0667
Zhang L, Sun T, Woldesellassie F, Xiao H, Tao Y (2015) Sex ratio meiotic drive as a plausible evolutionary mechanism for hybrid male sterility. PLoS Genet 11:e1005073. https://doi.org/10.1371/journal.pgen.1005073
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We thank the Department of Studies in Genetics and Genomics, University of Mysore for providing the infrastructure.
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This work was supported by Department of Biotechnology (DBT), Ministry of Science and Technology, Government of India to NBR (grant number BT/PR9871/BID/7/472/2013); We acknowledge Council of Scientific and Industrial Research (CSIR), Govt. of India for providing fellowship to RC.
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Chowdanayaka, R., Basappa, R.N. Rapid Divergence of Key Spermatogenesis Genes in nasuta-Subgroup of Drosophila. J Mol Evol 90, 2–16 (2022). https://doi.org/10.1007/s00239-021-10037-x
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DOI: https://doi.org/10.1007/s00239-021-10037-x