Copulatory wounding and traumatic insemination

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 5, 2015, Pages 1-26

  Reinhardt, Klaus ^a   Anthes, Nils ^a   Lange, Rolanda ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; CALLOSOBRUCHUS; CIMEX; COLEOPTERA; GASTROPODA;

ANIMAL; CLASSIFICATION; COPULATION; INSECT; PHYLOGENY; PHYSIOLOGY; SEXUAL BEHAVIOR;

ANIMALS; COPULATION; INSECTS; PHYLOGENY; SEXUAL BEHAVIOR, ANIMAL;

EID: 84930466199     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a017582     Document Type: Article

References (155)

1. Adamo SA. 1999. Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Anim Behav 57: 117–124.
2. Alexander RD, Marshall DC, Cooley JR. 1997. Evolutionary perspectives on insect mating. In Mating systems in insects and arachnids (ed. Choe JC, Crespi BJ), pp. 4–31. Cambridge University Press, Cambridge.
3. Anderson SL, Sheridan DJ. 2012. Female genital injury following consensual and nonconsensual sex: State of the science. J Emerg Nurs 38: 518–522.
4. Anderson SL, Parker BJ, Bourguignon CM. 2008. Changes in genital injury patterns over time in women after consensual intercourse. J Forensic Leg Med 15: 306–311.
5. Anderson SL, Parker BJ, Bourguignon CM. 2009. Predictors of genital injury after nonconsensual intercourse. Adv Emerg Nurs J 31: 236–247.
6. Anthes N. 2010. Mate choice and reproductive conflict in simultaneous hermaphrodites.In Animal behaviour: Evolution and mechanisms (ed. Kappeler P), pp. 329–357. Springer, Berlin.
7. Anthes N, Michiels NK. 2007a. Precopulatory stabbing, hypodermic injections and unilateral matings in a hermaphroditic sea slug. Biol Lett 3: 121–124.
8. Anthes N, Michiels NK. 2007b. Reproductive morphology, mating behaviour, and spawning ecology of cephalaspid sea slugs (Aglajidae and Gastropteridae). Invert Biol 126: 335–365.
9. Arnqvist G. 1998. Comparativeevidence for the evolution of genitalia by sexual selection. Nature 393: 784–786.
10. Arnqvist G, Nilsson T. 2000. The evolution of polyandry: Multiple mating and female fitness in insects. Anim Be-hav 60: 145–164.
11. Arnqvist G, Rowe L. 2002a. Antagonistic coevolution between the sexes in a group of insects. Nature 415: 787–789.
12. Arnqvist G, Rowe L. 2002b. Correlated evolution of male and female morphologies in water striders. Evolution 56: 936–947.
13. Arnqvist G, Thornhill R. 1998. Evolution of animal genita-lia: Patterns of phenotypic and genotypic variation and condition dependence of genital and non-genital morphology in water striders (Heteroptera: Gerridae: In-secta). Genet Res 71: 193–212.
14. Astrup BS, Ravn P, Lauritsen J, Thomsen JL. 2012. Nature, frequency and duration ofgenital lesions after consensual sexual intercourse—Implications for legal proceedings. Forensic Sci Int 219: 50–56.
15. Backhouse A, Sait SM, Cameron TC. 2012. Multiple mating in the traumatically inseminating Warehouse pirate bug, Xylocoris flavipes: Effects on fecundity and longevity. Biol Lett 8: 706–709.
16. Baminger H, Locher R, Baur B. 2000. Incidence of dart shooting, sperm delivery, and sperm storage in natural populations of the simultaneously hermaphroditic land snail Arianta arbustorum. Can J Zool 78: 1767–1774.
17. Bateman AJ. 1948. Intra-sexual selection in Drosophila. Heredity 2: 349–368.
18. Beani L, Giusti F, Mercati D, Lupetti P, Paccagnini E, Turil-lazzi S, Dallai R. 2005. Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited.J Morphol 265: 291–303.
19. Benoit JB, Jajack AJ, Yoder JA. 2012. Multiple traumatic insemination events reduce the abilityof bed bug females to maintain water balance. J Comp Physiol B 182: 189–198.
20. Berkowitz CD. 2011. Healing of genital injuries. J Child Sex Abuse 20: 537–547.
21. Bieman DN, Witter JA. 1982. Mating wounds in Malaco-soma: An insight into bed bug mating-behavior. Fla En-tomol 65: 377–378.
22. Blanckenhorn WU, Hosken DJ, Martin OY, Reim C, Teuschl Y, Ward PI. 2002. The costs of copulating in the dung fly Sepsis cynipsea. Behav Ecol 13: 353–358.
23. Carayon J. 1966a. Traumatic insemination and the paragen-ital system. In Monograph of Cimicidae (ed. Usinger RL), pp. 81–166. Thomas Say Foundation, Entomological Society of America, College Park, MD.
24. Carayon J. 1966b. Les inseminations traumatiques acciden-telles chez certains Hémiptères Cimicoidea [Accidental traumatic insemination in some Hemiptera Cimicoidea]. CR Acad Sc Paris 262: 2176–2179.
25. Carayon J. 1974. Etude sur les Hémiptères Plokiophilidae [Study on the Hemiptera Plokiophilidae]. Ann Soc Fr (NS) 10: 499–525.
26. Carayon J. 1977. Insémination extra-génitale traumatique. In Traite des zoologie–Anatomie, systématique, biologie— Tome VIII Fascicule V-A—Insectes: Gamétogenèses, fécon-dation, metamorphoses [Extragenital traumatic insemination. In Textbook of zoology–Anatomy, systematics, biology–Vol VIII Part V-A–Insects: Gametogenesis, fertilization, metamorphoses] (ed. Grassé PP), pp. 351–390. Masson, Paris.
27. Cayetano L, Maklakov AA, Brooks RC, Bonduriansky R. 2011. Evolution of male and female genitalia following release from sexual selection. Evolution 65: 2171–2183.
28. Chapman T, Partridge L. 1996. Female fitness in Drosophila melanogaster: An interaction between the effect of nutrition and of encounter rate with males. Proc R Soc B 263: 755–759.
29. Chase R, Vaga K. 2006. Independence, not conflict, characterizes dart-shooting and sperm exchange in a hermaphroditic snail. Behav Ecol Sociobiol 59: 732–739.
30. Clutton-Brock TH. 1984. Reproductive effort and terminal investment in iteroparous animals. Am Nat 123: 219–229.
31. Clutton-Brock TH, Parker GA. 1995. Sexual coercion in animal societies. Anim Behav 49: 1345–1365.
32. Coomans A, Verschuren D, Vanderhaeghen R. 1988. The demanian system, traumatic insemination and reproductive strategy in Oncholaimus oxyuris Ditlevsen (Nema-toda, Oncholaimina). Zool Scr 17: 15–23.
33. Cordero C, Miller JS. 2012. On the evolution and function of caltrop cornuti in Lepidoptera—Potentially damaging male genital structures transferred to females during copulation. J Nat Hist 46: 701–715.
34. Cordero Rivera A, Andres JA, Cordoba-Aguilar A, Utzeri C. 2004. Postmating sexual selection: Allopatric evolution of sperm competition mechanisms and genital morphology in calopterygid damselflies (Insecta: Odonata). Evolution 58: 349–359.
35. Coyne JA. 2000. Of vice and men. The fairy tales of evolutionary psychology. New Republic 3: 27–34.
36. Coyne JA, Berry A. 2000. Rape as an adaptation. Is this contentious hypothesis advocacy, not science? Nature 404: 121–122.
37. Credland PF, Wright AW. 1989. Factors affecting female fecundity in the cowpea seed beetle, Callosobruchus mac-ulatus (Coleoptera: Bruchidae). J Stored Prod Res 25: 125–136.
38. Crudgington HS, Siva-Jothy MT. 2000. Genital damage, kicking and early death. Nature 407: 855–856.
39. Davey KG. 1960. The evolution of spermatophores in insects. Proc R Entomol Soc Lond A Gen Entomol 35: 107–113.
40. Davies NT. 1966. Reproductive physiology. In Monograph of Cimicidae (Hemiptera-Heteroptera) (ed. Usinger RL). Thomas Say Foundation, Entomological Society of America, College Park, MD.
41. Domanitskaya EV, Liu H, Chen S, Kubli E. 2007. The hy-droxyproline motif of male sex peptide elicits the innate immune response in Drosophila females. FEBS J 274: 5659–5668.
42. Eberhard WG. 1985. Sexual selection and animal genitalia. Harvard University Press, Cambridge, MA.
43. Eberhard WG. 1996. Female control: Sexual selection by cryptic female choice. Princeton University Press, Princeton, NJ.
44. Eberhard WG. 2006. Sexually antagonistic coevolution in insects is associated with only limited morphological diversity. J Evol Biol 19: 657–681.
45. Eberhard WG, Huber BA, Rodriguez RLS, Briceno RD, Salas I, Rodriguez V. 1998. One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution 52: 415–431.
46. Edgardh K, von Krogh G, Ormstad K. 1999. Adolescent girls investigated for sexual abuse: History, physical findings and legal outcome. Forensic Sci Int 104: 1–15.
47. Edvardsson M, Tregenza T. 2005. Why do male Callosobru-chus maculatus harm their mates? Behav Ecol 16: 788–793.
48. Eke N. 2002. Urological complications of coitus. BJU Int 89: 273–277.
49. Fornoni J.2011. Ecological and evolutionary implications of plant tolerance to herbivory. Funct Ecol 25: 399–407.
50. Fox CW. 1993. Multiple mating, lifetime fecundity and female mortality of the bruchid beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Funct Ecol 7: 203–208.
51. Franck P, Solignac M, Vautrin D, Cornuet JM, Koeniger G, Koeniger N. 2002. Sperm competition and last-male precedence in the honeybee. Anim Behav 64: 503–509.
52. Gavrilets S, Waxman D. 2002. Sympatric speciation by sexual conflict. Proc Natl Acad Sci 99: 10533–10538.
53. Geist RF. 1988. Sexually related trauma. Emerg Med Clin North Am 6: 439–466.
54. Gendrin M, Welchman DP, Poidevin M, Herve M, Lemaitre B. 2009. Long-range activation of systemic immunity through peptidoglycan diffusion in Drosophila. PLoS Pathog 5: e1000694.
55. 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.
56. Gromko MH, Pyle DW. 1978. Sperm competition, male fitness, and repeated mating by female Drosophila mela-nogaster. Evolution 32: 588–593.
57. Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnström A. 1994. Infectious diseases, reproductive effort and the cost of reproduction in birds. Phil Trans R Soc Lond B 346: 323–331.
58. Haine ER, Rolff J, Siva-Jothy MT. 2007. Functional consequences of blood clotting in insects. Dev Comp Immunol 31: 456–464.
59. Heming BS. 2003. Insect development and evolution. Cornell University Press, Ithaca, NY.
60. Hosken DJ, Stockley P. 2004. Sexual selection and genital evolution. Trends Ecol Evol 19: 87–93.
61. Hotzy C, Arnqvist G. 2009. Sperm competition favors harmful males in seed beetles. Curr Biol 19: 404–407.
62. Hotzy C, Polak M, Ro¨nn JL, Arnqvist A. 2012. Phenotypic engineering unveils the function of genital morphology. Curr Biol 22: 2258–2261.
63. House CM, Simmons LW. 2005. The evolution of male gen-italia: Patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus. J Evol Biol 18: 1281–1292.
64. House CM, Lewis Z, Hodgson DJ, Wedell N, Sharma MD, Hunt J, Hosken DJ. 2013. Sexual and natural selection both influence male genital evolution. PLoS ONE 8: e63807.
65. Izquierdo MA, Rubio GD. 2011. Male genital mutilation in the high-mountain goblin spider, Unicorn catleyi. J Insect Sci 11: 118.
66. Johnstone RA, Keller L. 2000. How males can gain by harming their mates: Sexual conflict, seminal toxins, and the cost of mating. Am Nat 156: 368–377.
67. Jolivet P. 2008. Inverted copulation. In Encyclopedia of entomology (ed. Capinera JL), pp. 2014–2044. Springer, New York.
68. Jones JS, Rossman L, Hartman M, Alexander CC. 2003. Anogenital injuries in adolescents after consensual sexual intercourse. Acad Emerg Med 10: 1378–1383.
69. Jones JS, Rossman L, Diegel R, Van Order P, Wynn BN. 2009. Sexual assault in postmenopausal women: Epidemiology and patterns of genital injury. Am J Emerg Med 27: 922–929.
70. Kamimura Y. 2003. Effects of broken male intromittent organs on the sperm storage capacity of female earwigs, Euborellia plebeja. J Ethol 21: 29–35.
71. Kamimura Y. 2007. Twin intromittent organs of Drosophila for traumatic insemination. Biol Lett 3: 401–404.
72. Kamimura Y. 2010. Copulation anatomy of Drosophila mel-anogaster (Diptera: Drosophilidae): Wound-making organs and their possible roles. Zoomorphology 129: 163–174.
73. Kamimura Y. 2012. Correlated evolutionary changes in Dro-sophila female genitalia reduce the possible infection risk caused by male copulatory wounding. Behav Ecol Socio-biol 66: 1107–1114.
74. Kamimura Y, Lee C-Y. 2014. Mating and genital coupling in the primitive earwig species Echinosoma denticulatum (Pygidicranidae): Implications for genital evolution in dermapteran phylogeny. Arthrop Syst Phylog 72: 11–21.
75. Kamimura Y, Mitsumoto H. 2011. Comparative copulation anatomy of the Drosophila melanogaster species complex (Diptera: Drosophilidae). Entomol Sci 14: 399–410.
76. Kamimura Y, Mitsumoto H. 2012. Genital coupling and copulatory wounding in Drosophila teissieri (Diptera: Drosophilidae). Can J Zool 90: 1437–1440.
77. Kelly DL, Larkin HJ, Cosby CD, Paolinetti LA. 2013. Derivation of the Genital Injury Severity Scale (GISS): A concise instrument for description and measurement of external female genital injury after sexual intercourse. J Forensic Leg Med 20: 724–731.
78. Koene JM, Schulenburg H. 2005. Shooting darts: Co-evolution and counter-adaptation in hermaphroditic snails. BMC Evol Biol 5: 25.
79. Kramer AC. 2011. Penile fracture seems more likely during sex under stressful situations. J Sex Med 8: 3414–3417.
80. Lange R, Gerlach T, Beninde J, Werminghausen J, Reichel V, Anthes N. 2012. Female fitness optimum at intermediate mating rates under traumatic mating. PLoS ONE 7: e43234.
81. Lange R, Reinhardt K, Michiels NK, Anthes N. 2013a. Functions, mechanisms, and evolution of traumatic mating. Biol Rev 88: 585–601.
82. Lange R, Werminghausen J, Anthes A. 2013b. Does traumatic secretion transfer manipulate mating roles or reproductive output in a hermaphroditic sea slug? Behav Ecol Sociobiol 67: 1239–1247.
83. Lange R, Werminghausen J, Anthes N. 2014. Cephalo-trau-matic secretion transfer in a hermaphrodite sea slug. R Soc Lond B 281: 20132424.
84. Lee J, Singh B, Kravets FG, Trocchia A, Waltzer WC, Khan SA. 2000. Sexually acquired vascular injuries of the penis: A review. J Trauma 49: 351–358.
85. Lefevre G Jr, Jonsson UB. 1962. Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 47: 1719–1736.
86. Leonard JL, Pearse JS, Harper AB. 2002. Comparative reproductive biology of Ariolimax californicus and A. dolichophallus (Gastropoda: Stylommatophora). Invert Reprod Dev 41: 83–93.
87. Lessells CM. 2006. The evolutionaryoutcome of sexual conflict. Phil Trans R Soc Lond B 361: 301–317.
88. Lincoln C, Perera R, Jacobs I, Ward A. 2013. Macroscopically detected female genital injury after consensual and non-consensual vaginal penetration: A prospective comparison study. J Forensic Leg Med 20: 884–901.
89. Little TJ, Kraaijeveld AR. 2004. Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol Evol 19: 58–60.
90. Lockhart AB, Thrall PH, Antonovics J. 1996 Sexually transmitted diseases in animals: Ecological and evolutionary implications. Biol Rev 71: 415–471.
91. Mann T. 1984. Spermatophores: Development, structure, biochemical attributes, and role in the transfer of spermatozoa. Springer, New York.
92. 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.
93. McNeil CL, Bain CL, Macdonald SJ. 2011. Multiple quantitative trait loci influence the shape of a male-specific genital structure in Drosophila melanogaster. G3 (Bethes-da) 1: 343–351.
94. Medzhitov R, Schendier DS, Soares MP. 2012. Disease tolerance as a defense strategy. Science 335: 936–941.
95. Mehta SD, Moses S, Agot K, Parker CB, Ndinya-Achola JO, Maclean I, Bailey RC. 2009. Adult male circumcision does not reduce risk of incident Neisseria gonorrhoeae, Chlamydia trachomatis, or Trichomonas vaginalis infection: Results from a randomized controlled trial inKenya. J Infect Dis 200: 370–378.
96. Mehta SD, Krieger JN, Agot K, Moses S, Ndinya-Achola JO, Parker C, Bailey RC. 2010. Circumcision and reduced risk of self-reported penile coital injuries: Results from a randomized controlled trial in Kisumu, Kenya. J Urol 184: 203–209.
97. Mehta SD, Moses S, Parker CB, Agot K, Maclean I, Bailey RC. 2012. Circumcision status and incident herpes simplex virus type 2 infection, genital ulcer disease, and HIV infection. AIDS 26: 1141–1149.
98. Michiels NK. 1998. Mating conflicts and sperm competition in simultaneous hermaphrodites. In Sperm competition and sexual selection (ed. Birkhead TR, Møller AP), pp. 219–254. Academic, San Diego.
99. Moret Y, Schmid-Hempel P. 2000. Survival for immunity: The price of immune system activation for bumblebee workers. Science 290: 1166–1168.
100. Morrow EH, Arnqvist G. 2003. Costly traumatic insemination and a female counter-adaptation in bed bugs. Proc R Soc Lond B 270: 2377–2381.
101. Morrow EH, Innocenti P. 2012. Female postmating immune responses, immune system evolution and immunogenic males. Biol Rev 87: 631–638.
102. Morrow EH, Arnqvist G, Pitnick S. 2003. Adaptation versus pleiotropy: Why do males harm their mates? Behav Ecol 14: 802–806.
103. Müller HJ. 1962. Die variabilita¨t der genitalstrukturen bei zikaden und ihre biologische und taxonomische bedeu-tung [The variability of genitalic structures in planthop-pers and its biological and taxonomic significance]. Mittbl Insektenkd 6: 36–42.
104. Nessler SH, Uhl G, Schneider JM. 2007. Genital damage in the orb-web spider Argiope bruennichi (Araneae: Aranei-dae) increases paternity success. Behav Ecol 18: 174–181.
105. Neufeld CJ, Palmer AR. 2008. Precisely proportioned: Inter-tidal barnacles alter penis form to suit coastal wave action. Proc R Soc Lond B 275: 1081–1087.
106. Oliveira RF, Taborsky M, Brockmann HJ. 2008. Alternative reproductive tactics: An integrative approach. Cambridge University Press, Cambridge.
107. Otti O, Naylor R, Siva-Jothy MT, Reinhardt K. 2009. Bacte-riolytic activity in the ejaculate of an insect. Am Nat 174: 292–295.
108. Otti O, McTighe AP, Reinhardt K. 2013. In vitro antimicrobial sperm protection by an ejaculate-like substance. Funct Ecol 27: 219–226.
109. Ozorak A, Hoşcan MB, Oksay T, Güzel A, Koşar A. 2014. Management and outcomes of penile fracture: 10 years’ experience from atertiary care center. Int Urol Nephrol 46: 519–522.
110. Parker GA. 1979. Sexual selection and sexual conflict. In Sexual selection and reproductive competition in insects (ed. Blum MS, Blum NA), pp. 123–163. Academic, New York.
111. Parzer HF, Moczek AP. 2008. Rapid antagonistic coevolution between primary and secondary sexual characters in horned beetles. Evolution 62: 2423–2428.
112. Peng J, Zipperlen P, Kubli E. 2005. Drosophila sex-peptide stimulates female innate immune system after mating via Toll and Imd pathways. Curr Biol 15: 1690–1694.
113. Polanco A, Miller D, Brewster C. 2011. Reproductive potential of field-collected populations of Cimex lectularius L. and the cost of traumatic insemination. Insects 2: 326–335.
114. Proctor HC. 1998. Indirect sperm transfer in arthropods: Behavioural and evolutionary trends. A Rev Entomol 43: 153–174.
115. Pyle DW, Gromko MH. 1978. Repeated mating by female Drosophila melanogaster: The adaptive importance. Ex-perientia 34: 449–450.
116. Reaney LT, Knell RJ. 2010. Immune activation but not male quality affects female current reproductive investment in a dung beetle. Behav Ecol 21: 1367–1372.
117. Reichel V. 2011. “Penis morphology, mating strategies and fitness effects in simultaneous hermaphrodites.” Diploma thesis, Eberhard Karls Universität, Tübingen, Germany, pp. 1–48.
118. Reinhardt K. 2010. Natural selection and genital variation: A role for the environment, parasites and sperm ageing? Genetica 138: 119–127.
119. Reinhardt K, Jacobs DS. 2006. Abundance of Cacodmus vil-losus (Sta˚l, 1855) (Heteroptera: Cimicidae) on its host, Neoromica capensis (Chiroptera: Verspertillionidae). Afr Entomol 14: 398–400.
120. Reinhardt K, Naylor RA, Siva-Jothy MT. 2003. Reducing a cost of traumatic insemination: Female bed bugs evolve a unique organ. Proc R Soc Lond B 270: 2371–2375.
121. Reinhardt K, Naylor RA, Siva-Jothy MT. 2005. Potential sexual transmission of environmental microbes in a traumatically inseminating insect. Ecol Entomol 30: 607–611.
122. Reinhardt K, Harney E, Naylor R, Gorb S, Siva-Jothy MT. 2007. Female-limited polymorphism in the copulatory organ of a traumatically inseminating insect. Am Nat 170: 931–935.
123. Reinhardt K, Naylor RA, Siva-Jothy MT. 2009a. Ejaculate components delay reproductive senescence while elevating female reproductive rate in an insect. Proc Natl Acad Sci 106: 21743–21747.
124. Reinhardt K, Naylor RA, Siva-Jothy MT. 2009b. Situation exploitation: Higher male mating success when female resistance is reduced by feeding. Evolution 63: 29–39.
125. Reinhardt K, Naylor RA, Siva-Jothy MT. 2011. Male mating rate is constrained by seminal fluid availability in bedbugs, Cimex lectularius. PLoS ONE 6: e22082.
126. Rice WR. 1998. Speciation by sexual conflict. In Endless forms: Species and speciation (ed. Howard DJ, Berlocher SH), pp. 261–270. Oxford University Press, Oxford.
127. Rice WR, Chippendale A. 2001. Intersexual ontogenetic conflict. JEvol Biol 14: 685-693.
128. Riggs N, Houry D, Long G, Markovchick V, Feldhaus KM. 2000. Analysis of 1,076 cases of sexual assault. Ann Emerg Med 35: 358-362.
129. Ronn JL, Hotzy C. 2012. Do longer genital spines in male seed beetles function as better anchors during mating? Anim Behav 83: 75-79.
130. Ronn J, Katvala M, Arnqvist G. 2007. Coevolution between harmful male genitalia and female resistance in seed beetles. Proc Natl Acad Sci 104: 10921-10925.
131. Scharer L, Janick T, Ramm SA. 2014. Sexual conflict in hermaphrodites. Cold Spring Harb Perspect Biol doi:10.1101/cshperspect.a017673.
132. Sekizawa A, Seki S, Tokuzato M, Shiga S, Nakashima Y 2013. Disposable penis and its replenishment in a simultaneous hermaphrodite. Biol Lett 9: 20121150.
133. Shapiro JP, Shirk PD, Kelley K., Lewis TM, Horton DR. 2010. Identity of two sympatric species of Orius (Hemiptera: Heteroptera: Anthocoridae). J Insect Sci 10: 189.
134. Siva-Jothy MT. 2009. Reproductive immunity. In Insect infection and immunity (ed. Rolff J, Reynolds SE), pp. 241-250. Oxford University Press, Oxford.
135. Siva-Jothy MT, Moret Y, Rolff J. 2005. Insect Immunity: An evolutionary ecology perspective. Adv Insect Physiol 32: 1–48.
136. Smolensky N, Romero MR, Krug PJ. 2009. Evidence for costs of mating and self-fertilization in a simultaneous hermaphrodite with hypodermic insemination, the Opisthobranch Alderia willowi. Biol Bull 216: 188-199.
137. Sota T, Kubota K. 1998. Genital lock-and-key as a selective agent against hybridization. Evolution 52: 1507–1513.
138. Stockley P. 2002. Sperm competition risk and male genital anatomy: Comparative evidence for reduced duration of female sexual receptivity in primates with penile spines. Evol Ecol 16: 123-137.
139. Stutt AD, Siva-Jothy MT. 2001. Traumatic insemination and sexual conflict in the bed bug Cimex lectularius. Proc Natl Acad Sci 98: 5683-5687.
140. Szabo R, Short RV. 2000. How does male circumcision protect against HIV infection? Brit Med J 320: 1592-1594.
141. Tatarnic NJ, Cassis G. 2013. Surviving in sympatry: Para-genital divergence and sexual mimicry between a pair of traumatically inseminating plant bugs. Am Nat 182: 542–551.
142. Tatarnic NJ, Cassis G, Siva-Jothy MT. 2014. Traumatic insemination in terrestrial arthropods. A Rev Entomol 59: 245–261.
143. Theopold U, Schmidt O, Söderhall K, Dushay MS. 2004. Coagulation in arthropods: Defence, wound closure and healing. Trends Immunol 25: 289–294.
144. Uhl G, Nessler SH, Schneider JM. 2010. Securing paternity in spiders: A review on occurrence and effects of mating plugs and male genital mutilation. Genetica 138: 75–104.
145. Ullyot P, Beauchamp RSA. 1931. Mechanisms for the prevention of self-fertilization in some species of fresh-water triclads. Q J Microsc Sci 74: 477–490.
146. Usinger RL. 1966. Monograph of Cimicidae (Hemiptera-Het-eroptera), Vol. 7. Thomas Say Foundation, Entomological Society of America, College Park, MD.
147. Valdes A. 2004. Morphologyof the penial hooks and vaginal cuticular lining of some dorid nudibranchs (Mollusca, Opisthobranchia). Am Malacol Bull 18: 49–53.
148. Watanabe S, Hara M, Watanabe Y. 2000. Male internal fertilization and introsperm-like sperm of the seaweed pipefish (Syngnathus schlegeli). Zool Sci 17: 759–767.
149. West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford University Press, Oxford.
150. Wilson CJ, Tomkins JL. 2014. Countering counteradapta-tions: Males hijack control of female kicking behavior. Behav Ecol 25: 470–476.
151. Wilson N, Tufton TJ, Eady PE. 1999. The effect of single, double, and triple matings on the lifetime fecundity of Callosobruchus analis and Callosobruchus maculatus (Co-leoptera: Bruchidae). J Insect Behav 12: 295–306.
152. Yassin A, Orgogozo V. 2013. Coevolution between male and female genitalia in the Drosophila melanogaster species subgroup. PLoS ONE 8: e57158.
153. Yip A, Ng SK, Wong WC, Li MK, Lam KH. 1989. Injury to the prepuce. Br J Urol 63: 535–538.
154. Zaher H. 1999. Hemipenial morphologyofthe South American xenodontine snakes: With a proposal for a mono-phyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bull Am Mus Nat Hist 240: 1–168.
155. Zhong W, McClure CD, Evans CR, Mlynski DT, Immonen E, Ritchie MG, Priest NK. 2014. Immune anticipation of mating in Drosophila: Turandot M promotes immunity against sexually transmitted fungal infections. Proc R Soc B 280: 20132018.