2.2 Violent mating: traumatic insemination in bed bugs and other  (Page 6/6)

However, what is interesting to note is that while a male who mates with a virgin female bed bug has a significantly longer copulation duration and ejaculate size than a male who mates with the female afterwards, the latter actually has a higher fertilization success, with a 68% last-male sperm precedence in C. lectularius after two matings (Stutt&Siva-Jothy 2001). One explanation for the longer copulation duration between a male and a virgin female is that it is possible the first male’s ejaculate is subjected to disproportionate phagocytic attack from hemocytes in the female’s spermalege. Therefore, selection via sperm competition may favor first males who have a large ejaculate size (Siva-Jothy&Stutt 2003).

Conclusion: evolutionary significance of traumatic insemination

Consistent to the evolutionary arms race theory, both male and female bed bugs have evolved certain adaptations and counter-adaptations against each other in order to optimize their own reproductive fitness (Morrow et al. 2003). Although the origins of traumatic insemination are unclear, many hypotheses have been proposed, including bypassing the mating plug and overcoming female resistance during copulation, which would be reproductively advantageous to males (Parker 2008). Although we may never know its origins, the studies surrounding traumatic insemination in C. lectularius have truly provided valuable insight into sexual conflict and further research should be conducted to get an even clearer picture.

Discussion questions:

1. Why is the spermalege considered a counteradaptation? In what ways does the spermalege benefit the female?
2. Can you think of a scenario in which the traumatic insemination and evolutionary arms race in the bed bug would be reversed due to selective pressures? In what scenario would increased matings benefit females?

Glossary

• Evolutionary Arms Race - The evolutionary struggle between competing sets of co-evolving genes that develop adaptations and counter-adaptations against each other.
• Ectospermalege - The cuticular groove that guides the male’s intromittent organ into the mesospermalege (Reinhardt&Siva-Jothy 2007).
• Hematophagous - Feeding on blood.
• Hemolymph - Found in organisms with open circulatory systems, hemolymph is comparable to the blood and lymph of vertebrates.
• Hemocoel - The cavity found in insects that contains the hemolymph.
• Intromittent organ - Refers to an external organ of a male organism that is used for delivering sperm during copulation, also known as paramere.
• Mating plug - A gelatinous secretion deposited by a male into a female genital tract that later prevents the female from being successfully bred with later (Parker 2008).
• Mesopermalege - The hemocyte-containing bed bug organ into which sperm are introduced (Reinhardt&Siva-Jothy 2007).
• Oviposition - a term used for invertebrates and especially insects, oviposition refers to the act of laying eggs.
• Paramere - see intromittent organ.
• Polyandry - A mating system in which one female copulates with multiple males.
• Sclerotized - Hardened by the presence of substances other than chitin, such as scleroproteins, waxes, or calcium salts
• Sexual conflict - occurs when the male and female have conflicting optimal fitness strategies concerning reproduction, leading to evolutionary arms race between the two sexes.
• Spermalege - consisting of the ectospermalege and mesospermalege, the spermalege is a pair of sperm-receptacles which reduce damage to the female bedbug during traumatic insemination.
• Sperm Precedence - an indicator of male fertilization success in a polygamous mating system.
• Traumatic insemination - the mating practice in some species of invertebrates in which the male pierces the female’s abdomen with an intromittent organ and injects sperm directly into the abdominal cavity.

References:

1. Arnqvist, G.,&Nilsson, T. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour. 60:145-164.

   In insects, although multiple mating in polyandry usually has a negative effect on the lifespan of females, the positive effects of increased rate of egg production and fertility outweigh negative, so polyandry has been selected for in insects.

2. Carayon, J. 1966. Traumatic insemination and the paragenital system. In: R. L. Usinger, Monograph of Cimicidae (Hemiptera-Heteroptera). College Park, MD: Entomological Society of America. p. 81-166.
3. Crudgington, H. S.,&Siva-Jothy, M. T. 2000. Genital damage, kicking and early death. Nature. 407: 855-856.
4. Dawkins, R.,&Krebs, J. R. 1979. Arms races between and within species. Proceedings of the Royal Society of London. Series B, Biological Sciences. 205: 489-511.

   Counter-adaptations arise in response to selection pressure, which generates an arms race.

5. Goddard, J,&deShazo, R. 2009. Bed bugs (Cimex lectularius) and clinical consequences of their bites. The Journal of the American Medical Association. 301: 1358-1366.
6. Hotzy, C.,&Arnqvist, G. 2009. Sperm competition favors harmful males in seed beetles. Current Biology. 19: 404-407.
7. Johnstone, R. A.,&Keller, L. 2000. How males can gain by harming their mates: sexual conflict, seminal toxins, and the cost of mating. The American Naturalist. 156: 368-377.

   Male bed bugs and other insects traumatically inseminate their partners mainly to stop or delay females from remating.

8. Kamimura, Y. 2007. Twin intromittent organs of Drosophila for traumatic insemination. Biology Letters. 3:401-04
9. Lessells, C. M. 2006. The evolutionary outcome of sexual conflict. Philosophical Transactions of the Royal Society B: Biological Sciences. 361: 301-317.
10. Morrow, E. H.,&Arnqvist, G. 2003. Costly traumatic insemination and a female counter-adaptation in bed bugs. Proceedings of the Royal Society B: Biological Sciences. 270: 2377–2381.

    Costs of traumatic insemination to female bed bugs were determined by varying the rate of insemination as well as the rate and mode of piercing trauma to females, with the results providing evidence that the spermalege is a female counter-adaption to a sexually anatogonistic male trait.

11. Morrow, E. H., Arnqvist, G.,&Pitnick, S. 2003. Adaptation versus pleiotropy: why do males harm their mates?. International Society for Behavioral Ecology. 14: 802-806.
12. Newberry, K. 2008. The effects on domestic infestations of Cimex lectularius bedbugs of interspecific mating with C. hemipterus. Medical and Veterinary Entomology. 3: 407-414.
13. Otti, O., Naylor, R., Siva-Jothy, M.T.&Reinhardt, K. 2009. Bacteriolytic activity in the ejaculate of an insect. American Naturalist. 174: 292-295
14. Panagiotakopulu, E.,&Buckland P.C. 1999. Cimex lectularius L., the common bed bug from Pharaonic Egypt. Antiquity. 73: 908-11.
15. Parker, G. A. 2008. Sperm competition and its evolutionary consequences in the insects. Biological Reviews. 45: 525-567.
16. Polak, M.,&Rashed, A. 2010. Microscale laser surgery reveals adaptive function of male intromittent genitalia. Proceedings of the Royal Society B: Biological Sciences. 1-6.
17. Reinhardt, K., Harney, E., Naylor, R., Gorb, S.,&Siva-Jothy, M. T. 2007. Female-limited polymorphism in the copulatory organ of a traumatically inseminating insect. The American Naturalist. 170: 931-935.
18. Reinhardt, K., Naylor, R.,&Siva-Jothy, M. T. 2003. Reducing a cost of traumatic insemination: female bedbugs evolve a unique organ. Proceedings of the Royal Society B: Biological Sciences. 270: 2371-2375.

    Female bed beg bugs have evolved a spermalege, an organ that serves as a counter-adaptation against male intromittent organs by reducing the costs of mating associated infection.

19. Reinhardt, K., Naylor, R. A.,&Siva-Jothy, M. T. 2005. Potential sexual transmission of environmental microbes in a traumatically inseminating insect. Ecological Entomology. 30: 607-611.

    During traumatic insemination, harmful microbes enter the female bed bug, which leave her susceptible to infection and even death.

20. Reinhardt, K., Naylor, R. A.,&Siva-Jothy, M. T. 2009a. Situation exploitation: higher male mating success when female resistance is reduced by feeding. Evolution. 63: 29-39.
21. Reinhardt, K.,&Siva-Jothy, M. T. 2007. Biology of bed bugs (Cimicidae). Annual Review of Entomology. 52: 351-374.
22. Reinhardt, K., Wong, C. H.,&Georgiou, A. S. 2009b. Seminal fluid proteins in the bed bug, Cimex lectularius, detected using two-dimensional gel electrophoresis and mass spectrometry. Parisitology. 136: 283-292.
23. Rezac, M. 2009. The spider Harpactea sadistica: co-evolution of traumatic insemination and complex female genital morphology in spiders. The Proceedings of the Royal Society B: Biological Sciences. 276: 2697-2701.
24. Rice, W. R.,&Holland, B. 1997. The enemies within: intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behavioral Ecology and Sociobiology. 41: 1-10.

    Antagonistic co-evolution is common among loci that code for social interactions.

25. Ronn, J., Katvala, M.,&Arnqvist, G. 2007. Coevolution between harmful male genitalia and female resistance in seed beetles. Proceedings of the National Academy of Sciences in the United States of America. 104: 10921-10925.
26. Simmons, L. W. 2001. Sperm competition and its evolutionary consequences in the insects. Princeton University Press.
27. Siva-Jothy, M. T. 2006. Trauma, disease and collateral damage: conflict in cimicids. Philosophical Transactions of the Royal Society B: Biological Sciences. 361: 269-275.

    Despite the presence of functional female genital tracts, cimicids reproduce by traumatic insemination.

28. Siva-Jothy, M. T.,&Stutt, A. D. 2003. A matter of taste: direct detection of female mating status in the bedbug. Articles from Proceedings of the Royal Society B: Biological Sciences. 270: 649-652.

    In bed bugs, mating duration is directly related to ejaculate size and a female’s first copulation always lasts longer than subsequent ones, providing evidence that males can sense the mating status of the female.

29. Stutt, A. D.,&Siva-Jothy, M. T. 2001. Traumatic insemination and sexual conflict in the bed bug Cimex lectularius. Proceedings of the National Academy of Sciences of the United States of America. 98: 5683-5687.

    Traumatic insemination in bed bugs results in last-male sperm precedence, suboptimal remating frequencies in females, and reduced longevity and reproductive success in females.

30. Tatarnic, N. J., Cassis, G.,&Hochuli, D. F. 2006. Traumatic insemination in the plant bug genus Coridromius Signoret (Heteroptera: Miridae). Biology Letters. 2: 58-61.
31. Usinger, R. L. 1966. Monograph of Cimicidae (Hemiptera-Heteroptera). College Park, MD: Entomological Society of America.
32. Wigby, S.,&Chapman, T. 2004. Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution. 58: 1028-1037.

Biography

Christine Sun was born in Gaithersburg, MD and currently attends Rice University in Houston, TX. There, she is a sophomore double majoring in Biochemistry and Asian Studies. She loves to travel, and recently came back from a service trip to Taiwan. It was actually because of the numerous bed bug bites she received in Taiwan that compelled her to go to Wikipedia to research bed bugs in the first place. Although she does not think bed bugs are the most pleasant creatures, she finds their reproductive behavior fascinating.