Intraspecific sperm competition genes enforce post-mating species barriers in Drosophila

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1797, 2014, Pages

  Castillo, Dean M ^a   Moyle, Leonie C ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Reproductive isolation; Sexual selection; Sperm competition

Indexed keywords

CONSPECIFIC; FLY; INTRASPECIFIC COMPETITION; REPRODUCTIVE ISOLATION; SEXUAL CONFLICT; SEXUAL SELECTION; SPERM COMPETITION;

DROSOPHILA PROTEIN;

ANIMAL; DROSOPHILA; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; MALE; PHYSIOLOGY; REPRODUCTION; SEXUAL BEHAVIOR; SPECIES DIFFERENCE; SPERMATOZOON;

ANIMALS; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SPECIES SPECIFICITY; SPERMATOZOA;

EID: 84908374413     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.2050     Document Type: Article

References (42)

1. Arnqvist G, Edvardson M, Friberg U, Nilsson T. 2000 Sexual conflict promotes speciation in insects. Proc. Natl Acad. Sci. USA 97, 10460–10464. (doi:10.1073/pnas.97.19.10460)
2. Panhuis TM, Butlin R, Zuk M, Tregenza T. 2001 Sexual selection and speciation. Trends Ecol. Evol. 16, 364–371. (doi:10.1016/S0169-5347(01)02160-7)
3. Ritchie MG. 2007 Sexual selection and speciation. Annu. Rev. Ecol. Evol. Syst. 38, 79–102. (doi:10.1146/annurev.ecolsys.38.091206.095733)
4. Kirkpatrick M, Ravigne V. 2002 Speciation by natural and sexual selection: models and experiments. Am. Nat. 159, S22–S35. (doi:10.1086/338370)
5. Gavrilets S, Hayashi TI. 2005 Speciation and sexual conflict. Evol. Ecol. 19, 167–198. (doi:10.1007/s10682-004-7916-4)
6. Chenoweth SF, McGuigan K. 2010 The genetic basis of sexually selected variation. Annu. Rev. Ecol. Evol. Syst. 41, 81–101. (doi:10.1146/annurev-ecolsys-102209-144657)
7. Arbuthnott D. 2009 The genetic architechture of insect sourtship behavior and premating isolation. Heredity 103, 15–22. (doi:10.1038/hdy.2009.22)
8. Groot AT et al. 2013 One quantitative trait locus for intra-and interspecific variation in a sex pheromone. Mol. Ecol. 22, 1065–1080. (doi:10.1111/mec.12171)
9. Ryan MJ, Rand AS. 1993 Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47, 647–657. (doi:10. 2307/2410076)
10. Bolnick DI, Kirkpatrick M. 2012 The relationship between intraspecific assortative mating and reproductive isolation between divergent populations. Curr. Zool. 58, 484–492.
11. Findlay GD, Yi X, MacCoss MJ, Swanson WJ. 2008 Proteomics reveals novel Drosophila seminal fluid proteins transferred at mating. PLoS Biol. 6, e178. (doi:10.1371/journal.pbio.0060178)
12. Findlay GD, MacCoss MJ, Swanson WJ. 2009 Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome Res. 19, 886–896. (doi:10.1101/gr.089391.108)
13. Sirot LK, LaFlamme BA, Sitnik JL, Rubinstein CD, Avila FW, Chow CY, Wolfner MF. 2009 Molecular social interactions: Drosophila melanogaster seminal fluid proteins as a case study. In Socio-genetics (ed. MB Sokolowski), pp. 23–56. Waltham, MA: Academic Press.
14. Chow CY, Wolfner MF, Clark AG. 2001 The genetic basis for male x female interactions underlying variation in reproductive phenotypes of Drosophila. Genetics 186, 1355–1365. (doi:10.1534/genetics.110.123174)
15. Begun DJ, Whitley P, Todd BL, Waldrip-Dail HM, Clark AG. 2000 Molecular population genetics of male accessory gland proteins in Drosophila. Genetics 156, 1879–1888.
16. Wong A, Turchin MC, Wolfner MF, Aquadro CF. 2008 Evidence for positive selection on Drosophila melanogaster seminal fluid protease homologs. Mol. Biol. Evol. 25, 497–506. (doi:10.1093/molbev/msm270)
17. Snook RR, Chapman T, Moore PJ, Wedell N, Crudgington HS. 2009 Interactions between the sexes: new perspectives on sexual selection and reproductive isolation. Evol. Ecol. 23, 71–91. (doi:10.1007/s10682-007-9215-3)
18. Price CSC. 1997 Conspecific sperm precedence in Drosophila. Nature 388, 663–666. (doi:10.1038/41753)
19. Howard DJ. 1999 Conspecific sperm and pollen precedence and speciation. Annu. Rev. Ecol. Evol.Syst. 30, 109–132. (doi:10.1146/annurev.ecolsys.30.1.109)
20. Gioti A, Wigby S, Wertheim B, Schuster E, Martinez P, Pennington CJ, Partridge L, Chapman T. 2012 Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females. Proc. R. Soc. B 279, 4423–4432. (doi:10.1098/rspb.2012.1634)
21. Avila FW, Ravi Ram K, Qazi MCB, Wolfner MF. 2010 Sex peptide is required for the efficient release of stored sperm in mated Drosophila females. Genetics 186, 595–600. (doi:10.1534/genetics.110.119735)
22. Liu H, Kubli E. 2003 Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 100, 9929–9933. (doi:10.1073/pnas.1631700100)
23. Chapman T, Bangham J, Vinti G, Seifried B, Lung O, Wolfner MF, Smith HK, Partridge L. 2003 The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc. Natl Acad. Sci. USA 100, 9923–9928. (doi:10.1073/pnas.1631635100)
24. Ravi Ram K, Wolfner MF. 2007 Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins. PLoS Genet. 3, e238. (doi:10.1371/journal.pgen.0030238)
25. Ravi Ram K, Wolfner MF. 2009 A network of interactions among seminal proteins underlies the long-term postmating response in Drosophila. Proc. Natl Acad. Sci. USA 106, 15384–15389. (doi:10.1073/pnas.0902923106)
26. Neubaum DM, Wolfner MF. 1999 Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 153, 845–857.
27. Chapman T, Neubaum DM, Wolfner MF, Partridge L. 2000 The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster. Proc. R. Soc. Lond. B 267, 1097–1105. (doi:10.1098/rspb.2000.1114)
28. Holtzman S, Miller D, Eisman R, Kuwayama H, Niimi T, Kaufman T. 2010 Transgenic tools for members of the genus Drosophila with sequenced genomes. Fly 4, 349–362. (doi:10.4161/fly.4.4.13304)
29. Pyle DW, Gromko MH. 1981 Genetic basis for repeated mating in Drosophila melanogaster. Am. Nat. 117, 133–146. (doi:10.1086/283694)
30. Markow TA, O’Grady PM. 2005 Drosophila: a guide to species identification and use, 1st edn. Waltham, MA: Academic Press.
31. Findlay GD, Sitnik JL, Wang W, Aquadro CF, Clark NL, Wolfner MF. 2014 Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses. PLoS Genet. 10, e1004108. (doi:10.1371/journal.pgen.1004108)
32. Yang Z. 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591. (doi:10.1093/molbev/msm088)
33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013 MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729. (doi:10.1093/molbev/mst197)
34. Heger A, Ponting CP. 2007 Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes. Genome Res. 17, 1837–1849. (doi:10.1101/gr.6249707)
35. Britch SC, Swartout EJ, Hampton DD, Draney ML, Chu J, Marshall JL, Howard DJ. 2007 Genetic architecture of conspecific sperm precedence in Allonemobius fasciatus and A. socius. Genetics 176, 1209–1222. (doi:10.1534/genetics.106.064949)
36. Levesque L, Brouwers B, Sundararajan V, Civetta A. 2010 Third chromosome candidate genes for conspecific sperm precedence between D. simulans and D. mauritiana. BMC Genet. 11, 12. (doi:10.1186/1471-2156-11-21)
37. Wiernasz DC, Kingsolver JG. 1991 Wing melanin pattern mediates intraspecific mate choice and species recognition in Pontia occidentalis. Anim. Behav. 42, 276–280.
38. Williams TH, Gumm JM, Mendelson TC. 2013 Sexual selection acting on a speciation trait in darters (Percidae: Etheostoma). Behav. Ecol. 24, 1407–1414. (doi:10.1093/beheco/art080)
39. Sæther SA et al. 2007 Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318, 95–97. (doi:10.1126/science.1141506)
40. Parnell NF, Streelman JT. 2013 Genetic interactions controlling sex and color establish the potential for sexual conflict in Lake Malawi cichlid fishes. Heredity 110, 239–246. (doi:10.1038/hdy.2012.73)
41. Manier MK, Belote JM, Berben KS, Lüpold S, Ala-Honkola O, Collins WF, Pitnick S. 2013 Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution 67, 2348–2362. (doi:10.1111/evo.12117)
42. Manier MK, Lüpold S, Belote JM, Starmer WT, Berben KS, Ala-Honkola O, Collins WF, Pitnick S. 2013 Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Curr. Biol. 23, 1853–1862. (doi:10.1016/j.cub. 2013.07.086)