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Sexual Conflict in Water Striders, Dragonflies and Diving Beetles

  • Adolfo Cordero-RiveraEmail author
  • Anais Rivas-Torres
Chapter

Abstract

The field of sexual selection has been historically dominated by a stereotyped view of the sexual roles, with competing males and selective females, but in recent decades there has been a paradigm switch, with the emergence and dominance of the concept of sexual conflict. Put simply, there is sexual conflict when the optimum value for a trait (or a group of traits) is different for females and males. Although the recent literature mainly considers sexual conflict as a process separate from the other well-known processes in the field of postcopulatory sexual selection (sperm competition and cryptic female choice), our approach is that sexual conflict is the consequence of several pressures related to natural and sexual selection, and not a process by itself. Therefore, here we consider sexual conflict as a part of a continuum of sexual selection mechanisms. We concentrate on the effects of sexual conflict on reproductive behaviour of three groups of aquatic insects, whose habitats differ markedly, water striders, odonates and diving beetles, but also include some examples of studies addressing sexual conflict in other groups of aquatic insects. Our hypothesis is that the dimensional structure of the habitat will affect the intensity of sexual conflict over mating rate, copulation duration and postcopulatory guarding. There is abundant evidence and comprehensive reviews of the conflict over mating rates in water striders, odonates and, to a lesser degree, diving beetles. The bi-dimensionality of the water surface allows an easy monopolisation of females by males in this microhabitat, and water striders conform to this rule, so that the commonest mating system is characterised by strong conflicts and struggles before and after copulation. For animals like odonates, which are fast fliers and can use diverse terrestrial microhabitats, the opportunities for males to force females to copulate are certainly limited. In the case of diving beetles, the situation seems more favourable for the females, as they could control male approaches by hiding easily in the vegetation, or even in the case of extreme male density they could fly away and move to a different water body. The sexual conflict over mating duration is also intense in water striders, and also relevant in the other reviewed groups. In the field of postcopulatory conflicts, odonates have offered the best examples of male adaptations and female counter-adaptations, which are even more elaborated when studying the evolution of genitalia. We end by summarising our main conclusions and propose some ideas for future work. We stress that a comprehensive understanding of sexual conflicts in animals requires the study of both male and female anatomies, as well as their behaviours, avoiding assumptions or gender stereotypes, which have historically biased research to a male-view approach.

Keywords

Behaviour Equity Cryptic female choice Sperm competition 

Notes

Acknowledgements

Funding was provided by a grant from the Spanish Ministry of Economy and Competitiveness, including FEDER funds (CGL2014-53140-P). ART was supported by a FPI grant (BES-2015-071965).

References

  1. Ah-King M, Barron AB, Herberstein ME (2014) Genital evolution: why are females still understudied? PLoS Biol 12:1–7.  https://doi.org/10.1371/journal.pbio.1001851 CrossRefGoogle Scholar
  2. Aiken RB (1992) The mating behaviour of a boreal water beetle, Dytiscus alaskanus (Coleoptera Dytiscidae). Ethol Ecol Evol 4:245–254.  https://doi.org/10.1080/08927014.1992.9523136 CrossRefGoogle Scholar
  3. Alcock J (1979) Multiple mating in Calopteryx maculata (Odonata: Calopterygidae) and the advantage of non-contact guarding by males. J Nat Hist 13:439–446CrossRefGoogle Scholar
  4. Alcock J (1982) Postcopulatory mate guarding by males of the damselfly Hetaerina vulnerata Selys (Odonata: Calopterygidae). Anim Behav 30:99–107CrossRefGoogle Scholar
  5. Alcock J (1994) Postinsemination associations between males and females in insects: The mate guarding hypothesis. Annu Rev Entomol 39:1–21CrossRefGoogle Scholar
  6. Amano H, Hayashi K, Kasuya E (2008) Avoidance of egg parasitism through submerged oviposition by tandem pairs in the water strider, Aquarius paludum insularis (Heteroptera: Gerridae). Ecol Entomol 33:560–563.  https://doi.org/10.1111/j.1365-2311.2008.00988.x CrossRefGoogle Scholar
  7. Andrés JA, Cordero-Rivera A (2000) Copulation duration and fertilization success in a damselfly: An example of cryptic female choice? Anim Behav 59:695–703PubMedCrossRefGoogle Scholar
  8. Arnqvist G (1997) The evolution of water strider mating systems: causes and consequences of sexual conflicts. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 146–163CrossRefGoogle Scholar
  9. Arnqvist G, Danielsson I (1999) Copulatory behavior, genital morphology, and male fertilization success in water striders. Evolution 53:147–156PubMedCrossRefPubMedCentralGoogle Scholar
  10. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164PubMedCrossRefPubMedCentralGoogle Scholar
  11. Arnqvist G, Rowe L (2002) Correlated evolution of male and female morphologies in water striders. Evolution 56:936–947.  https://doi.org/10.1554/0014-3820(2002)056[0936:CEOMAF]2.0.CO;2 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonCrossRefGoogle Scholar
  13. Arnqvist G, Jones TM, Elgar MA (2006) Sex-role reversed nuptial feeding reduces male kleptoparasitism of females in Zeus bugs (Heteroptera; Veliidae). Biol Lett 2:491–493.  https://doi.org/10.1098/rsbl.2006.0545 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Baker RR (1983) Insect territoriality. Annu Rev Entomol 28:65–89CrossRefGoogle Scholar
  15. Bañuelos Irusta J, Araújo A (2007) Reproductive tactics of sexes and fitness in the dragonfly, Diastatops obscura. J Insect Sci 7:24Google Scholar
  16. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368PubMedCrossRefGoogle Scholar
  17. Brennan PLR, Prum RO (2015) Mechanisms and evidence of genital coevolution: the role of natural selection, mate choice, and sexual conflict. In: Rice WR, Gavrilets S (eds) The genetics and biology of sexual conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 385–413Google Scholar
  18. Byers CJ, Eason PK (2009) Conspecifics and their posture influence site choice and oviposition in the damselfly Argia moesta. Ethology 115:721–730CrossRefGoogle Scholar
  19. Campbell V, Fairbairn DJ (2001) Prolonged copulation and the internal dynamics of sperm transfer in the water strider Aquarius remigis. Can J Zool 79:1801–1812.  https://doi.org/10.1139/cjz-79-10-1801 CrossRefGoogle Scholar
  20. Carranza J (2009) Defining sexual selection as sex-dependent selection. Anim Behav 77:749–751CrossRefGoogle Scholar
  21. Cassis G, Hodgins M, Weir TA, Tatarnic NJ (2018) Phylogenetic reclassification and genitalic morphology of the small water strider genus Nesidovelia Andersen & Weir and allied Microveliinae (Hemiptera:Veliidae). Aust Entomol 57:92–106.  https://doi.org/10.1111/aen.12273 CrossRefGoogle Scholar
  22. Cleavall L (2009) Description of Thermonectus nigrofasciatus and Rhantus binotatus (Coleoptera: Dytiscidae) mating behavior. University of New Mexico, AlbuquerqueGoogle Scholar
  23. Clutton BTH, Parker G (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365CrossRefGoogle Scholar
  24. Corbet PS (1957) The life-history of the Emperor dragonfly Anax imperator Leach (Odonata: Aeshnidae). J Anim Ecol 26:1–69CrossRefGoogle Scholar
  25. Corbet PS (1962) A biology of dragonflies. Classey (fac-simile 1983), FaringdomGoogle Scholar
  26. Cordero A (1989) Reproductive behaviour of Ischnura graellsii (Rambur) (Zygoptera: Coenagrionidae). Odonatologica 18:237–244Google Scholar
  27. Cordero A (1990) The adaptive significance of the prolonged copulations of the damselfly, Ischnura graellsii (Odonata: Coenagrionidae). Anim Behav 40:43–48CrossRefGoogle Scholar
  28. Cordero A (1992) Sexual cannibalism in the damselfly species Ischnura graellsii (Odonata: Coenagrionidae). Entomol Gen 17:17–20CrossRefGoogle Scholar
  29. Cordero A (1999) Forced copulations and female contact guarding at a high male density in a Calopterygid damselfly. J Insect Behav 12:27–37CrossRefGoogle Scholar
  30. Cordero A, Andrés JA (2002) Male coercion and convenience polyandry in a Calopterygid damselfly (Odonata). J Insect Sci 2:14. Available online: insectscience.org/2.14 CrossRefGoogle Scholar
  31. Cordero Rivera A, Córdoba-Aguilar A (2016) Selección postcópula: competencia espermática. In: Etología adaptativa: el comportamiento como producto de la selección natural. p 479–504Google Scholar
  32. Cordero A, Santolamazza-Carbone S, Utzeri C (1992) A twenty-four-hours-lasting tandem in Coenagrion scitulum (Ramb.) in the laboratory (Zygoptera: Coenagrionidae). Not Odonatol 3:166–167Google Scholar
  33. Cordero A, Santolamazza-Carbone S, Utzeri C (1998) Mating opportunities and mating costs are reduced in androchrome female damselflies, Ischnura elegans (Odonata). Anim Behav 55:185–197PubMedCrossRefPubMedCentralGoogle Scholar
  34. Cordero-Rivera A (2002) Influencia de la selección sexual sobre el comportamiento reproductor de los odonatos. In: Evolución: la base de la biología. p 497–507Google Scholar
  35. Cordero-Rivera A (2016) Sperm removal during copulation confirmed in the oldest extant damselfly, Hemiphlebia mirabilis. Peer J 4:e2077.  https://doi.org/10.7717/peerj.2077 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Cordero-Rivera A (2017a) Behavioral diversity (ethodiversity): a neglected level in the study of biodiversity. Front Ecol Evol 5:1–7.  https://doi.org/10.3389/fevo.2017.00007 CrossRefGoogle Scholar
  37. Cordero-Rivera A (2017b) Sexual conflict and the evolution of genitalia: male damselflies remove more sperm when mating with a heterospecific female. Sci Rep 7:7844.  https://doi.org/10.1038/s41598-017-08390-3 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Cordero-Rivera A, Córdoba-Aguilar A (2010) Selective forces propelling genitalic evolution in Odonata. In: Leonard J, Córdoba-Aguilar A (eds) The evolution of primary sexual characters in animals. Oxford University Press, Oxford, pp 332–352Google Scholar
  39. Cordero-Rivera A, Egido Pérez FJ (1998) Mating frequency, population density and female polychromatism in the damselfly _Ischnura graellsii_: an analysis of four natural populations. Etología 6:61–67Google Scholar
  40. Cordero-Rivera A, Zhang H (2018) Ethological uniqueness of a damselfly with no near relatives: the relevance of behaviour as part of biodiversity. Anim Biodivers Conserv 41:161–174CrossRefGoogle Scholar
  41. Cordero-Rivera A, Utzeri C, Santolamazza-Carbone S (1999) Emergence and adult behaviour of Macromia splendens (Pictet) in Galicia, northwestern Spain (Anisoptera: Corduliidae). Odonatologica 28:333–342Google Scholar
  42. Cordero-Rivera A, Andrés JA, Córdoba-Aguilar A, Utzeri C (2004) Postmating sexual selection: allopatric evolution of sperm competition mechanisms and genital morphology in calopterygid damselflies (Insecta: Odonata). Evolution 58:349–359PubMedCrossRefPubMedCentralGoogle Scholar
  43. Córdoba-Aguilar A (2000) Reproductive behaviour of the territorial damselfly Calopteryx haemorrhoidalis asturica Ocharan (Zygoptera: Calopterygidae). Odonatologica 29:295–305Google Scholar
  44. Córdoba-Aguilar A (2006) Sperm ejection as a possible cryptic female choice mechanism in Odonata (Insecta). Physiol Entomol 31:146–153CrossRefGoogle Scholar
  45. Córdoba-Aguilar A, Cordero-Rivera A (2008) Cryptic female choice and sexual conflict. In: Córdoba-Aguilar A (ed) Dragonflies and damselflies. Model organisms for ecological and evolutionary research. Oxford University Press, Oxford, pp 189–202CrossRefGoogle Scholar
  46. Córdoba-Aguilar A, Uhía E, Cordero Rivera A (2003) Sperm competition in Odonata (Insecta): the evolution of female sperm storage and rivals’ sperm displacement. J Zool 261:381–398.  https://doi.org/10.1017/S0952836903004357 CrossRefGoogle Scholar
  47. Córdoba-Aguilar A, Serrano-Meneses MA, Cordero-Rivera A (2009) Copulation duration in nonterritorial odonate species lasts longer than in territorial species. Ann Entomol Soc Am 102:694–701.  https://doi.org/10.1603/008.102.0414 CrossRefGoogle Scholar
  48. Córdoba-Aguilar A, Vrech DE, Rivas M et al (2015) Allometry of male grasping apparatus in odonates does not suggest physical coercion of females. J Insect Behav 28:15–25CrossRefGoogle Scholar
  49. Daly M (1978) The cost of mating. Am Nat 112:771–774CrossRefGoogle Scholar
  50. Dawkins R (1976) The selfish gene. Oxford University Press, OxfordGoogle Scholar
  51. Dettner K, Schwinger G (1980) Defensive substances from pygidial glands of water beetles. Biochem Syst Ecol 8:89–95.  https://doi.org/10.1016/0305-1978(80)90032-0 CrossRefGoogle Scholar
  52. Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, CambridgeCrossRefGoogle Scholar
  53. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  54. Eberhard WG (2006) Sexually antagonistic coevolution in insects is associated with only limited morphological diversity. J Evol Biol 19:657–681PubMedCrossRefPubMedCentralGoogle Scholar
  55. Eberhard WG (2010) Evolution of genitalia: theories, evidence, and new directions. Genetica 138:5–18PubMedCrossRefPubMedCentralGoogle Scholar
  56. Fairn ER, Schulte-Hostedde AI, Alarie Y (2007) Sexual selection on accessory glands, genitalia and protarsal pads in the whirligig beetle Dineutus nigrior Roberts (Coleoptera: Gyrinidae). Ethology 113:257–266CrossRefGoogle Scholar
  57. Fincke OM (1986) Underwater oviposition in a damselfly (Odonata: Coenagrionidae) favors male vigilance, and multiple mating by females. Behav Ecol Sociobiol 18:405–412CrossRefGoogle Scholar
  58. Fincke OM (1997) Conflict resolution in the Odonata: implications for understanding female mating patterns and female choice. Biol J Linn Soc 60:201–220CrossRefGoogle Scholar
  59. Fincke OM (2004) Polymorphic signals of harassed female odonates and the males that learn them support a novel frequency-dependent model. Anim Behav 67:833–845CrossRefGoogle Scholar
  60. Guignot F (1933) Les Hydrocanthares de France. Les Frères Douladoure, ToulouseGoogle Scholar
  61. Heberdey RF (1931) Zur Entwicklungsgeschichte, Vergleichenden Anatomie und Physiologie der Weiblichen Geschlechtsausführwege der Insekten. Zeitschrift für Morphol und Ökologie der Tiere 22:416–586CrossRefGoogle Scholar
  62. Higginson DM, Pitnick S (2011) Evolution of intra-ejaculate sperm interactions: do sperm cooperate? Biol Rev 86:249–270.  https://doi.org/10.1111/j.1469-185X.2010.00147.x CrossRefPubMedPubMedCentralGoogle Scholar
  63. Higginson DM, Miller KB, Segraves KA, Pitnick S (2012a) Female reproductive tract form drives the evolution of complex sperm morphology. Proc Natl Acad Sci 109:4538–4543.  https://doi.org/10.1073/pnas.1111474109 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Higginson DM, Miller KB, Segraves KA, Pitnick S (2012b) Convergence, recurrence and diversification of complex sperm traits in diving beetles (Dytiscidae). Evolution 66:1650–1661.  https://doi.org/10.1111/j.1558-5646.2011.01532.x CrossRefPubMedPubMedCentralGoogle Scholar
  65. Hirayama H, Kasuya E (2008) Factors affecting submerged oviposition in a water strider: level of dissolved oxygen and male presence. Anim Behav 76:1919–1926.  https://doi.org/10.1016/j.anbehav.2008.08.013 CrossRefGoogle Scholar
  66. Keffer SL (2004) Morphology and evolution of water scorpion male genitalia (Heteroptera: Nepidae). Syst Entomol 29:142–172.  https://doi.org/10.1111/j.0307-6970.2004.00236.x CrossRefGoogle Scholar
  67. Koch K (2006) Effects of male harassment on females’ oviposition behaviour in Libellulidae (Odonata). Int J Odonatol 9:71–80.  https://doi.org/10.1080/13887890.2006.9748264 CrossRefGoogle Scholar
  68. Latty TM (2006) Flexible mate guarding tactics in the dragonfly Sympetrum internum (Odonata: Libellulidae). J Insect Behav 19:469–477.  https://doi.org/10.1007/s10905-006-9037-0 CrossRefGoogle Scholar
  69. Lauer MJ, Sih A, Krupa JJ (1996) Male density, female density and inter-sexual conflict in a stream-dwelling insect. Anim Behav 52:929–939.  https://doi.org/10.1006/anbe.1996.0241 CrossRefGoogle Scholar
  70. Leonard JL, Córdoba-Aguilar A (2010) The evolution of primary sexual characters in animals. Oxford University Press, OxfordGoogle Scholar
  71. Lindeboom M (1998) Post-copulatory behaviour in Calopteryx females (Insecta, Odonata, Calopterygidae). Int J Odonatol 1:175–184CrossRefGoogle Scholar
  72. Liu X, Hayashi F, Lavine LC, Yang D (2015) Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts? Proc R Soc B Biol Sci.  https://doi.org/10.1098/rspb.2015.0247 PubMedCrossRefPubMedCentralGoogle Scholar
  73. Lorenzo-Carballa MO, Beatty CD, Utzeri C et al (2009) Parthenogenetic Ischnura hastata revisited: present status and notes on population ecology and behaviour (Odonata: Coenagrionidae). Int J Odonatol 12:395–411CrossRefGoogle Scholar
  74. Machado G, Trumbo ST (2018) Parental care. In: Córdoba-Aguilar A, González-Tokman D, González-Santoyo I (eds) Insect behavior. Oxford University Press, Oxford, pp 203–2018Google Scholar
  75. Madsen BL (2012) Submersion respiration in small diving beetles (Dytiscidae). Aquat Insects 34:57–76.  https://doi.org/10.1080/01650424.2012.643026 CrossRefGoogle Scholar
  76. Matsubara K, Hironaka M (2005) Postcopulatory guarding behaviour in a territorial damselfly, Pseudagrion p. pilidorsum (Brauer), for submerged ovipositing females (Zygoptera: Coenagrionidae). Odonatologica 34:387–396Google Scholar
  77. Milam EL (2010) Looking for a few good males, female choice in evolutionary biology. John Hopkins University Press, BaltimoreGoogle Scholar
  78. Miller PL (1987a) An examination of the prolonged copulations of Ischnura elegans (Vander Linden) (Zygoptera: Coenagrionidae). Odonatologica 16:37–56Google Scholar
  79. Miller PL (1987b) Sperm competition in Ischnura elegans (Vander Linden) (Zygoptera: Coenagrionidae). Odonatologica 16:201–207Google Scholar
  80. Miller KB (2001) On the phylogeny of the Dytiscidae (Insecta: Coleoptera) with emphasis on the morphology of the female reproductive system. Insect Syst Evol 32:45–92CrossRefGoogle Scholar
  81. Miller KB (2003) The phylogeny of diving beetles (Coleoptera: Dytiscidae) and the evolution of sexual conflict. Biol J Linn Soc 79:359–388CrossRefGoogle Scholar
  82. Miller KB, Bergsten J (2014) Predaceous diving beetle sexual systems. In: Yee DA (ed) Ecology, systematics, and the natural history of predaceous diving beetles (Coleoptera: Dytiscidae). Springer, Dordrecht, pp 199–233Google Scholar
  83. Opphenheimer SD, Waage JK (1987) Hand-pairing: a new technique for obtaining copulations within and between Calopteryx species (Zygoptera: Calopterygidae). Odonatologica 16:291–296Google Scholar
  84. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:535–567.  https://doi.org/10.1111/j.1469-185X.1970.tb01176.x CrossRefGoogle Scholar
  85. Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic Press, New York, pp 123–166Google Scholar
  86. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos Trans R Soc Lond B Biol Sci 361:235–259PubMedPubMedCentralCrossRefGoogle Scholar
  87. Perry JC, Rowe L (2018) Sexual conflict in its ecological setting. Philos Trans R Soc Lond B Biol Sci 373:20170418PubMedCrossRefPubMedCentralGoogle Scholar
  88. Perry JC, Garroway CJ, Rowe L (2017) The role of ecology, neutral processes and antagonistic coevolution in an apparent sexual arms race. Ecol Lett 20:1107–1117.  https://doi.org/10.1111/ele.12806 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Polhemus JT (1974) The austrina group of the genus Microvelia (Hemiptera; Veliidae). Gt Basin Nat 34:207–217Google Scholar
  90. Queller DC, Strassmann JE (2018) Evolutionary conflict. Annu Rev Ecol Evol Syst 49:73–93.  https://doi.org/10.1146/annurev-ecolsys-110617-062527 CrossRefGoogle Scholar
  91. Reinhardt K, Anthes N, Lange R (2014) Copulatory wounding and traumatic insemination. In: Rice WR, Gavrilets S (eds) The genetics and biology of sexual conflict. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 115–140Google Scholar
  92. Rowe RJ (1978) Ischnura aurora (Brauer), a dragonfly with unusual mating behaviour (Zygoptera: Coenagrionidae). Odonatologica 7:375–383Google Scholar
  93. Rowe L (1992) Convenience polyandry in a water strider: foraging conflicts and female control of copulation frequency and guarding duration. Anim Behav 44:189–202CrossRefGoogle Scholar
  94. Rowe L (1994) The costs of mating and mate choice in water striders. Anim Behav 48:1049–1056CrossRefGoogle Scholar
  95. Rowe L, Arnqvist G (2002) Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes. Evolution 56:754–767PubMedCrossRefPubMedCentralGoogle Scholar
  96. Rowe L, Arnqvist G, Sih A, Krupa J (1994) Sexual conflict and the evolutionary ecology of mating patterns: water striders as a model system. Trends Ecol Evol 9:289–293PubMedCrossRefPubMedCentralGoogle Scholar
  97. Rubenstein DI (1989) Sperm competition in the water strider, Gerris remigis. Anim Behav 38:631–636.  https://doi.org/10.1016/S0003-3472(89)80008-9 CrossRefGoogle Scholar
  98. Sánchez-Guillén RA, Córdoba-Aguilar A, Cordero-Rivera A, Wellenreuther M (2014) Rapid evolution of prezygotic barriers in non-territorial damselflies. Biol J Linn Soc 113:485–496CrossRefGoogle Scholar
  99. Santolamazza S, Baquero E, Cordero-Rivera A (2011) Incidence of Anagrus obscurus (Hymenoptera: Mymaridae) egg parasitism on Calopteryx haemorrhoidalis and Platycnemis pennipes (Odonata: Calopterygidae: Platycnemididae) in Italy. Entomol Sci 14:366–369.  https://doi.org/10.1111/j.1479-8298.2011.00454.x CrossRefGoogle Scholar
  100. Sattler W (1957) Beobachtungen zur Fortpflanzung von Gerris najas De Geer (Heteroptera). Zeitschrift für Morphol und Ökologie der Tiere 45:411–428CrossRefGoogle Scholar
  101. Schneider JM (2014) Sexual Cannibalism as a Manifestation of Sexual Conflict. Cold Spring Harb Perspect Biol 6(11):a017731.  https://doi.org/10.1101/cshperspect.a017731 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Sharp D, Muir F (1912) The comparative anatomy of the male genital tube in Coleoptera. Trans R Entomol Soc London 60:477–532CrossRefGoogle Scholar
  103. Shuker DM (2014) Sexual selection theory. In: Shuker DM, Simmons LW (eds) The evolution of insect mating systems. Oxford University Press, Oxford, pp 20–41CrossRefGoogle Scholar
  104. Simmons LW (2014) Sexual selection and genital evolution. Aust J Entomol 53:1–7CrossRefGoogle Scholar
  105. Spence JR, Anderson NM (1994) Biology of water striders: interactions between systematics and ecology. Annu Rev Entomol 39:101–128.  https://doi.org/10.1146/annurev.en.39.010194.000533 CrossRefGoogle Scholar
  106. Stoks R, De Bruyn L, Matthysen E (1997) The adaptiveness of intense contact mate guarding by males of the Emerald Damselfly, Lestes sponsa (Odonata, Lestidae): The male’s perspective. J Insect Behav 10:289–298CrossRefGoogle Scholar
  107. Thornhill R (1983) Cryptic female choice in the scorpionfly Harpobittacus nigriceps and its implications. Am Nat 122:765–788CrossRefGoogle Scholar
  108. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine, Chicago, pp 136–179Google Scholar
  109. Uhía E, Cordero-Rivera A (2005) Male damselflies detect female mating status: importance for postcopulatory sexual selection. Anim Behav 69:797–804CrossRefGoogle Scholar
  110. Utzeri C (1988) Female “refusal display” versus male “threat display” in Zygoptera: is it a case of intraspecific imitation? Odonatologica 17:45–54Google Scholar
  111. Utzeri C, Ercoli C (2004) Disturbance by unpaired males prolongs postcopulatory guarding duration in the damselfly Lestes virens (Charpentier) (Zygoptera: Lestidae). Odonatologica 33:291–301Google Scholar
  112. Van Gossum H, Sherratt TN, Cordero-Rivera A (2008) The evolution of sex-limited colour polymorphisms. In: Córdoba-Aguilar A (ed) Dragonflies and damselflies. Model organisms for ecological and evolutionary research. Oxford University Press, Oxford, pp 219–229CrossRefGoogle Scholar
  113. Waage JK (1979) Dual function of the damselfly penis: sperm removal and transfer. Science 203:916–918PubMedCrossRefPubMedCentralGoogle Scholar
  114. Waage JK (1984) Sperm competition and the evolution of odonate mating systems. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, Orlando, pp 251–290CrossRefGoogle Scholar
  115. Wilcox RS (1984) Male copulatory guarding enhances female foraging in a water strider. Behav Ecol Sociobiol 15:171–174.  https://doi.org/10.1007/BF00292971 CrossRefGoogle Scholar
  116. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar
  117. Yoshizawa K, Ferreira RL, Kamimura Y, Lienhard C (2014) Female penis, male vagina, and their correlated evolution in a cave insect. Curr Biol 24:1006–1010.  https://doi.org/10.1016/j.cub.2014.03.022 CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.ECOEVO Lab, EE Forestal, Campus UniversitarioPontevedraSpain

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