Coevolution between Male and Female Genitalia in the Drosophila melanogaster Species Subgroup

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Yassin, Amir ^a   Orgogozo, Virginie ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL STRUCTURES; ANIMAL TISSUE; ARTICLE; CERCAL TOOTH; COEVOLUTION; CONTROLLED STUDY; COPULATION; DEFENSE MECHANISM; DROSOPHILA; DROSOPHILA ERECTA; DROSOPHILA MAURITIANA; DROSOPHILA MELANOGASTER; DROSOPHILA ORENA; DROSOPHILA SANTOMEA; DROSOPHILA SECHELLIA; DROSOPHILA SIMULANS; DROSOPHILA TEISSIERI; DROSOPHILA YAKUBA; FEMALE; FEMALE GENITAL SYSTEM; MALE; MALE GENITAL SYSTEM; NONHUMAN; PHALLIC HOOK; PHALLIC SPINE; PHYLOGENY; SEX DIFFERENCE; SPECIES DIFFERENCE; SPERM LENGTH; SPERM STORAGE ORGAN SIZE; UROGENITAL SYSTEM PARAMETERS;

ANIMALS; BIOLOGICAL EVOLUTION; DROSOPHILA MELANOGASTER; FEMALE; GENITALIA, FEMALE; GENITALIA, MALE; MALE; PHYLOGENY;

EID: 84874535685     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057158     Document Type: Article

References (68)

1. Eberhard WG (1985) Sexual Selection and Animal Genitalia. Harvard University Press. 256 p.
2. Eberhard WG, (2010) Evolution of genitalia: theories, evidence, and new directions. Genetica 138: 5-18 doi:10.1007/s10709-009-9358-y.
3. Stutt AD, Siva-Jothy MT, (2001) Traumatic insemination and sexual conflict in the bed bug Cimex lectularius. Proc Natl Acad Sci USA 98: 5683-5687 doi:10.1073/pnas.101440698.
4. Arnqvist G, Rowe L (2005) Sexual Conflict: Princeton University Press. 360 p.
5. Hosken DJ, Stockley P, Tregenza T, Wedell N, (2009) Monogamy and the battle of the sexes. Annu Rev Entomol 54: 361-378 doi:10.1146/annurev.ento.54.110807.090608.
6. Huber BA, (1999) Sexual selection in pholcid spiders (Araneae, Pholcidae): artful chelicerae and forceful genitalia. J Arachnol 27: 135-141.
7. Huber BA, (2003) Southern African pholcid spiders: revision and cladistic analysis of Quamtana gen. nov. and Spermophora Hentz (Araneae: Pholcidae), with notes on male-female covariation. Zool J Linn Soc 139: 477-527.
8. Huber BA, (2005) High species diversity, male-female coevolution, and metaphyly in Southeast Asian pholcid spiders: the case of Belisana Thorell 1898 (Araneae, Pholcidae). Zoologica 155: 1-126.
9. Eberhard WG, (2004) Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice. Evolution 58: 1947-1970.
10. Kulkarni CV (1940) On the systematic position, structural modifications, bionomics and development of a remarkable new family of cyprinodont fishes from the province of Bombay. Records of the Indian Museum: 379-423.
11. Pratt HL, (1979) Reproduction in the blue shark Prionace glauca. Fish Bull 77: 445-470.
12. Rönn J, Katvala M, Arnqvist G, (2007) Coevolution between harmful male genitalia and female resistance in seed beetles. Proc Natl Acad Sci USA 104: 10921-10925 doi:10.1073/pnas.0701170104.
13. Arnqvist G, Rowe L, (2002) Antagonistic coevolution between the sexes in a group of insects. Nature 415: 787-789 doi:10.1038/415787a.
14. Carayon J (1966) Traumatic insemination and paragenital system. In: Usinger RL, editor. Monograph of Cimicidae (Hemiptera, Heteroptera). Entomol Soc America. 88-166.
15. Brennan PLR, Prum RO, McCracken KG, Sorenson MD, Wilson RE, et al. (2007) Coevolution of male and female genital morphology in waterfowl. PLoS ONE 2: e418 doi:10.1371/journal.pone.0000418.
16. Evans JP, Gasparini C, Holwell GI, Ramnarine IW, Pitcher TE, et al. (2011) Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification. Proc Biol Sci 278: 2611-2620 doi:10.1098/rspb.2010.2453.
17. Simmons LW, Garcia-Gonzalez F, (2011) Experimental coevolution of male and female genital morphology. Nat Commun 2: 374 doi:10.1038/ncomms1379.
18. Vahed K (n.d.) Coercive copulation in the alpine bushcricket Anonconotus alpinus Yersin (Tettigoniidae: Tettigoniinae: Platycleidini). Ethology 108: 1065-1075.
19. Peretti AV, Willemart RH, (2006) Sexual coercion does not exclude luring behavior in the climbing camel-spider Oltacola chacoensis (Arachnida, Solifugae, Ammotrechidae). J Ethol 25: 29-39 doi:10.1007/s10164-006-0201-y.
20. Hrušková-Martišová M, Pekár S, Bilde T, (2010) Coercive copulation in two sexually cannibalistic camel-spider species (Arachnida: Solifugae). J Zool 282: 91-99 doi:10.1111/j.1469-7998.2010.00718.x.
21. Jagadeeshan S, Singh RS, (2006) A time-sequence functional analysis of mating behaviour and genital coupling in Drosophila: role of cryptic female choice and male sex-drive in the evolution of male genitalia. J Evol Biol 19: 1058-1070 doi:10.1111/j.1420-9101.2006.01099.x.
22. Eberhard W, Ramirez N, (2004) Functional morphology of the male genitalia of four species of Drosophila: Failure to confirm both lock and key and male-female conflict. Annls Entomol Soc Am 97: 1007-1017.
23. Dickson BJ, (2008) Wired for sex: the neurobiology of Drosophila mating decisions. Science 322: 904-909 doi:10.1126/science.1159276.
24. Kamimura Y, (2007) Twin intromittent organs of Drosophila for traumatic insemination. Biol Lett 3: 401-404 doi:10.1098/rsbl.2007.0192.
25. Kamimura Y, (2010) Copulation anatomy of Drosophila melanogaster (Diptera: Drosophilidae): wound-making organs and their possible roles. Zoomorphology 129: 163-174 doi:10.1007/s00435-010-0109-5.
26. Kamimura Y, Mitsumoto H, (2012) Lock-and-key structural isolation between sibling Drosophila species. Entomol Sci 15: 197-201 doi:10.1111/j.1479-8298.2011.00490.x.
27. Kamimura Y, (2012) Correlated evolutionary changes in Drosophila female genitalia reduce the possible infection risk caused by male copulatory wounding. Behav Ecol Sociobiol 66: 1107-1114 doi:10.1007/s00265-012-1361-0.
28. Lung O, Wolfner MF, (1999) Drosophila seminal fluid proteins enter the circulatory system of the mated female fly by crossing the posterior vaginal wall. Insect Biochem Mol Biol 29: 1043-1052 doi:10.1016/S0965-1748(99)00078-8.
29. Ottiger M, Soller M, Stocker RF, Kubli E, (2000) Binding sites of Drosophila melanogaster sex peptide pheromones. J Neurobiol 44: 57-71.
30. Robertson HM, (1988) Mating asymmetries and phylogeny in the Drosophila melanogaster species complex. Pacif. Sci. 42: 72-80.
31. Kamimura Y, Mitsumoto H, (2011) Comparative copulation anatomy of the Drosophila melanogaster species complex (Diptera: Drosophilidae). Entomol Sci 14: 399-410 doi:10.1111/j.1479-8298.2011.00467.x.
32. Tsacas L, (1971) Drosophila teissieri, nouvelle espèce africaine du groupe melanogaster et note sur deux autres espèces nouvelles pour l'Afrique (Dipt. Drosophilidae). Bull Soc Entomol Fr 76: 35-45.
33. Tsacas L, Lachaise D, (1974) Quatre nouvelles espèces de la Côte-d'Ivoire du genre Drosophila, groupe melanogaster, et discussion de l'origine du sous-groupe melanogaster (Diptera: Drosophilidae). Annls Univ Abidjan 7: 193-211.
34. Tsacas L, David J, (1974) Drosophila mauritiana n. sp. du groupe melanogaster de l'île Maurice. Bull Soc Ent Fr 79: 42-46.
35. Tsacas L, David J, (1978) Une septième espèce appartenant au sous-groupe Drosophila melanogaster Meigen: Drosophila orena spec. nov. du Cameroun. (Diptera: Drosophilidae). Beitr Ent 28: 179-181.
36. Tsacas L, Bächli G, (1981) Drosophila sechellia, n. sp., huitième espèce du sous-groupe melanogaster des Iles Sechelles (Diptera, Drosophilidae). Rev Fr Entomol 3: 146-150.
37. Lachaise D, Harry M, Solignac M, Lemeunier F, Bénassi V, et al. (2000) Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé. Proc Biol Sci 267: 1487-1495 doi:10.1098/rspb.2000.1169.
38. Bächli G, Vilela CR, Escher SA, Saura A, Bächli G, et al. (2004) The Drosophilidae (Diptera) of Fennoscandia and Denmark. Fauna Entomol Scand 39: 1-362.
39. Abramoff MD, Magalhães PJ, Ram SJ, (2004) Image processing with ImageJ. Biophotonics Internat 11: 36-42.
40. Pagel M, (1994) Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proc Biol Sci 255: 37-45.
41. Maddison WP, Maddison DR (2012) Mesquite: a modular system for evolutionary analysis. Version 2.75. Available:http://mesquiteproject.org.
42. Obbard DJ, Maclennan J, Kim K-W, Rambaut A, O'Grady PM, et al. (2012) Estimating divergence dates and substitution rates in the Drosophila phylogeny. Mol Biol Evol. 29: 3459-3473.
43. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical approach to multiple testing. J R Stat Soc B 57: 289-300.
44. Dalmasso C, Broët P, Moreau T, (2005) A simple procedure for estimating the false discovery rate. Bioinformatics 21: 660-668.
45. Coyne JA, (1983) Genetic basis of differences in genital morphology among three sibling species of Drosophila. Evolution 37: 1101-1118.
46. Coyne JA, Rux J, David JR, (1991) Genetics of morphological differences and hybrid sterility between Drosophila sechellia and its relatives. Genet Res 57: 113-122.
47. Liu J, Mercer JM, Stam LF, Gibson GC, Zeng ZB, et al. (1996) Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. Genetics 142: 1129-1145.
48. Macdonald SJ, Goldstein DB, (1999) A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics 153: 1683-1699.
49. Zeng Z-B, Liu J, Stam LF, Kao C-H, Mercer JM, et al. (2000) Genetic architecture of a morphological shape difference between two Drosophila species. Genetics 154: 299-310.
50. Masly JP, Dalton JE, Srivastava S, Chen L, Arbeitman MN, (2011) The genetic basis of rapidly evolving male genital morphology in Drosophila. Genetics 189: 357-374 doi:10.1534/genetics.111.130815.
51. Sánchez L, Santamaria P, (1997) Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics 147: 231-242.
52. Lachaise D, Capy P, Cariou M-L, Joly D, Lemeunier F, et al. (2004) Nine relatives from one African ancestor: population biology and evolution of the Drosophila melanogaster subgroup species. In: Singh RS, Uyenoyama MK (eds.) The Evolution of Population Biology. Cambridge University Press. 315-343.
53. Lachaise D, Lemeunier F, Veuille M, (1981) Clinal variations in male genitalia in Drosophila teissieri Tsacas. Am Nat 117: 600-608.
54. Joly D, Cariou M-L, Mhlanga-Mutangadura T, Lachaise D, (2010) Male terminalia variation in the rainforest dwelling Drosophila teissieri contrasts with the sperm pattern and species stability. Genetica 138: 139-152 doi:10.1007/s10709-009-9423-6.
55. Pitnick S, Markow T, Spicer GS, (1999) Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution 53: 1804-1822 doi:10.2307/2640442.
56. Miller GT, Pitnick S, (2002) Sperm-female coevolution in Drosophila. Science 298: 1230-1233 doi:10.1126/science.1076968.
57. Joly D, Schiffer M, (2010) Coevolution of male and female reproductive structures in Drosophila. Genetica 138: 105-118 doi:10.1007/s10709-009-9392-9.
58. Mueller JL, Page JL, Wolfner MF, (2007) An ectopic expression screen reveals the protective and toxic effects of Drosophila seminal fluid proteins. Genetics 175: 777-783 doi:10.1534/genetics.106.065318.
59. Avila FW, Ravi Ram K, Bloch Qazi MC, 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.
60. Dufour L, (1844) Anatomie générale des Diptères. Annls Sci Nat 1: 224-264.
61. Masly JP, (2012) 170 years of "Lock-and-Key": genital morphology and reproductive isolation. Internat J Evol Biol 2012: 1-10 doi:10.1155/2012/247352.
62. Llopart A, Lachaise D, Coyne JA, (2005) An anomalous hybrid zone in Drosophila. Evolution 59: 2602-2607.
63. Cariou ML, Silvain JF, Daubin V, Da Lage JL, Lachaise D, (2001) Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line. Mol Ecol 10: 649-660.
64. Acebes A, Cobb M, Ferveur J-F, (2003) Species-specific effects of single sensillum ablation on mating position in Drosophila. J Exp Biol 206: 3095-3100 doi:10.1242/jeb.00522.
65. Polak M, Rashed A, (2010) Microscale laser surgery reveals adaptive function of male intromittent genitalia. Proc Biol Sci 277: 1371-1376 doi:10.1098/rspb.2009.1720.
66. Grieshop K, Polak M, (2012) The precopulatory function of male genital spines in Drosophila ananassae [Doleschall] (Diptera: Drosophilidae) revealed by laser surgery. Evolution 66: 2637-2645 doi:10.1111/j.1558-5646.2012.01638.x.
67. Lang M, Orgogozo V, (2012) Distinct copulation positions in Drosophila pachea males with symmetric or asymmetric external genitalia. Contribs Zool 81: 87-94.
68. Ritchie MG, (2007) Sexual selection and speciation. Ann Rev Ecol Evol Syst 38: 79-102 doi:10.1146/annurev.ecolsys.38.091206.095733.