Abstract
A long-standing mystery in morphological evolution is why male genitalia tend to diverge more rapidly than other structures. One possible explanation of this trend is that male genitalia function as “internal courtship devices,” and are under sexual selection by cryptic female choice (CFC) to induce female responses that improve the male’s chances of fathering her offspring. Males of closely related species, which have species-specific genital structures, are thought to provide divergent stimulation. Testing this hypothesis has been difficult; the presumed genital courtship behavior is hidden from view inside the female; appropriate experimental manipulations of male and female genitalia are often technically difficult and seldom performed; and most studies of how the male’s genitalia interact with those of the female are limited to a single species in a given group, thus limiting opportunities for comparisons of species-specific structures. In this chapter, we summarize data from morphological, behavioral, and experimental studies of six species in the tsetse fly genus Glossina , including new X-ray recordings that allowed visualization of events inside the female during real time. Species-specific male genital structures perform dramatic, stereotyped, rhythmic movements , some on the external surface of the female’s abdomen and others within her reproductive tract. Counting conservatively, a female Glossina may sense stimuli from the male’s genitalia at up to 8 sites on her body during some stages of copulation. As predicted by CFC theory, these movements differ among closely related species; some of the species-specific male genital structures that are apparently designed to stimulate the female move with different rhythms against different portions of the female’s body in different species. In no case does female morphology show signs of counter adaptations to avoid or reduce male stimulation or to fit mechanically with male structures, as predicted by some alternative hypotheses to explain rapid divergent evolution of genitalia; for most male structures, the corresponding portion of the female is featureless and uniform in different species. Experimental modifications of one species-specific genital structure (the cercus), and of the possible female sense organs in the portion of the female that this male structure contacts during copulation, elicited female reproductive responses in two species (reductions in sperm transport, ovulation , and resistance to further copulations) that could result in cryptic female choice favoring this male structure.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Aksoy S, Chen X, Hypsa V (1997) Phylogeny and possible transmission routes of midgut-associated endosymbionts of tsetse (Diptera: Glossinidae). Ins Mol Biol 6:183–190
Alexander RD, Marshall DC, Cooley JR (1997) Evolutionary perspectives on insect mating. In: Choe J, Crespie B (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 4–31
Arnqvist G (2006) Sensory exploitation and sexual conflict. Philos Trans Roy Soc B 361:375–386
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, New Jersey
Briceño RD, Eberhard WG (2009a) Experimental modifications of male genitalia confirm cryptic female choice theory of genital evolution. J Evol Biol 22:1516–1525
Briceño RD, Eberhard WG (2009b) Experimental demonstration of possible cryptic female choice on male tsetse fly genitalia. J Ins Physiol 55:989–996
Briceño RD, Eberhard WG, Robinson A (2007) Copulation behavior of Glossina pallidipes (Diptera: Muscidae) outside and inside the female, and genitalic evolution. Bull Ent Res 97:1–18
Briceño RD, Wegrzynek D, Chinea-Cano E, Eberhard WG, dos Santos-Rolo T (2010) Movements and morphology under sexual selection: tsetse fly genitalia. Ethol Ecol Evol 22:385–391
Briceño RD, Eberhard WG, Chinea-Cano E, Wegrzynek D, dos Santos Rolo T (2015) Species specific behavioral differences in male tsetse fly genitalia behavior during copulation, with a discussion of genitalic evolution in Glossina. Ethol Ecol Evol
Buxton PA (1955) The natural history of tsetse flies. HK Lewis, London
Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47
Chen PS (1984) The functional morphology and biochemistry of insect male accessory glands and their secretions. Ann Rev Ent 29:233–255
Chen X, Li S, Aksoy S (1999) Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48:49–58
Christy JH (1995) Mimicry, mate choice, and the sensory trap hypothesis. Am Nat 146:171–181
Córdoba-Aguilar A (2005) Possible coevolution of male and female genital form and function in a calopterygid damselfly. J Evol Biol 18:132–137
Crudgington HS, Siva-Jothy MJ (2000) Genital damage, kicking and early death. Nature 407:855–856
Curtis CF, Langley PA, Trewern MA (1980) X-Chromosome involvement in male hybrid sterility from Glossina morsitans sub-species crosses. Heredity 45:405–410
Dodd CHW (1973) Control of the reproductive cycle in tsetse flies (Glossina spp.). PhD thesis, University Edinburgh
Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge
Eberhard WG (1994) Evidence for widespread courtship during copulation in 131 species of insects and spiders, and implications for cryptic female choice. Evolution 48:711–733
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, New Jersey
Eberhard WG (2002) The function of female resistance behavior: intromission by male coercion vs. female cooperation in sepsid flies (Dipera: Sepsidae). Rev Biol Trop 50:485–505
Eberhard WG (2004a) Male-female conflict and genitalia: failure to confirm predictions in insects and spiders. Biol Rev 79:121–186
Eberhard WG (2004b) Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice. Evolution 58:1947–1970
Eberhard WG (2009) Static allometry and animal genitalia. Evolution 63(1):48–66
Feldmann U, Dyck VA, Mattioli RC, Jannin J (2005) Potential impact of tsetse fly control involving the sterile insect technique. In: Robinson AS, Dyck VA, Hendrichs J (eds) Sterile insect technique principles and practice in area-wide integrated pest management. Springer, The Netherlands, pp 701–723
Flowers RW, Eberhard WG (2006) Fitting together: copulatory linking in some tropical Chrysomelidae. Rev Biol Trop 54:829–842
Gillot C, Langley PA (1981) The control of receptivity and ovulation in the tsetse fly, Glossina morsitans. Physiol Ent 6:269–281
Gooding RH, Krafsur ES (2005) Tsetse genetics: contributions to biology, systematic, and control of tsetse flies. Ann Rev Entomol 50:101–123
Hargrove JW (2012) Age-specific changes in sperm levels among female tsetse flies (Glossina spp.) with a model for the time course of insemination. Physiol Entomol 37:278–290
Holland B, Rice WR (1998) Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1–7
Hoppenheit A, Bauer B, Steuber S, Terhalle W, Diall O, Zessin KH, Clausen PH (2013) Multiple host feeding in Glossina palpalis gambiensis and Glossina tachinoides in Southeast Mali. Med Vet Entomol 27:222–225
Hosken D, Stockley P (2003) Sexual selection and genital evolution. Trends Ecol Evol 19:87–93
Huyton PM, Langley PA, Carlson AD, Schwartz M (1980) Specificity of contact sex pheromones in tsetse flies, Glossina spp. Physiol Entomol 5:253–264
International Glossina Genome Initiative (169 authors) (2014) Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis. Science 344:380–386
Jaensen T (1979a) Mating of males of Glossina pallidipes Austen (Diptera: Glossinidae). Bull Ent Res 69:573–588
Jaensen T (1979b) Mating behaviour of Glossina pallidipes Austen (Diptera: Glossinidae): duration of copulation, insemination and fecundity. Entomol Exp Appl 26:1–12
Kawooya J (1977) Demonstration of multiple insemination in females of Glossina morsitans Westwood, using a phenotypic marker Ocra. J Appl Entomol 84:321–327
Leonard J, Córdoba-Aguilar A (2010) The evolution of primary sexual characters in animals. Oxford University Press, New York
McAlpine JF (1989) Phylogeny and classification of the Muscomorpha. In: McAlpine JF, Wood DM (eds) Manual of nearctic Diptera. Monograph 32, vol 3. Research Branch Agriculture Canada, pp 1397–1518
Merritt D (1989) The morphology of the phallosome and accessory gland material transfer during copulation in the blowfly, Lucilia cuprina (Insecta, Diptera). Zoomorphology 108:359–366
Mulligan HW (1970) The African trypanosomiases. Allen and Unwin, London
Newstead R, Evans AM, Potts WH (1924) Guide to the study of tsetse-flies. Hodder and Stoughton Limited, London
Patton WS (1936) Studies on the higher Diptera of medical and veterinary importance. A revision of the species of the genus Glossina Wiedemann based on a comparative study of male and female terminalia. Ann Trop Med Paras 30:71–89
Pinhão RC, Grácio AJS (1973) The degree of spermathecal impregnation and the number of matings in Glossina austeni. Ann Inst Higiene Med Trop 1:103–106
Pollock JN (1970) Sperm transfer by spermatophore in Glossina austeni Newstead. Nature 225:1063–1064
Pollock JN (1974) Anatomical relations during sperm transfer in Glossina austeni Newstead (Glossinidae, Diptera). Trans Roy Ent Soc Lond 125:489–501
Popper K (1970) Objective knowledge: an evolutionary approach. Oxford University Press, New York
Potts WH (1970) Systematics and identification of Glossina. In: Mulligan HW (ed) The African trypanosomiases. Allen & Unwin, London, pp 243–273
Riemann JG, Thorson BJ (1969) Effect of male material on oviposition and mating by female house flies. Ann Ent Soc Am 62:828–834
Saunders DS (1970) Reproduction of Glossina. In: Mulligan W (ed) The African trypanosomiases. Allen & Unwin, London, pp 327–344
Saunders DS, Dodd CHW (1972) Mating, insemination, and ovulation in the tsetse fly, Glossina morsitans. J Ins Physiol 18:187–198
Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, New Jersey
Simmons LW (2014) Sexual selection and genital evolution. Austral Entom 53:1–17
Socha JJ, Westneat MW, Harrison JF, Waters JS, Lee WK (2007) Real-time phase-contrast x-ray imaging: a new technique for the study of animal form and function. BMC Biol 5:6
Squire FA (1951) Observations on mating scars in Glossina palpalis (RD) Bull Ent Res 42:601–604
Tobe SS, Langley PA (1978) Reproductive physiology of Glossina. Ann Rev Entomol 23:283–307
Vanderplank FL (1947) Experiments in the hybridization of tsetse-flies (Glossina, Diptera) and the possibility of a new method of control. Trans Roy Ent Soc Lond 98:1–18
Wall R, Langley PA (1993) The mating behavior of tsetse flies (Glossina): a review. Physiol Entomol 18:211–218
Acknowledgments
We acknowledge collaboration and assistance from A.S. Robinson, D. Wegrzynek, E. Chinea-Cano, T. Dos Santos Rolo, A. Markowicz, C. Streli, P. Wobrauschek, and the staff of the Forschungszentrum Karlsruhe, in particular Alexander Rack, Timm Weitkamp, Patrik Vagovic, and Tilo Baumbach. We thank the International Atomic Energy Agency for the use of flies and facilities, Rudolf Boigner and Carmen Marin for help in rearing flies, Anita Aisenberg, Yoshitaka Kamimura and an unusually thorough anonymous reviewer for helpful comments on the manuscript, D. Monty Wood for advice on morphological homologies, Maribelle Vargas for help obtaining SEM images, and Jorge Hendrichs, Andrew Parker and Marc Vreysen for logistic support. The IAEA, STRI, and the Universidad de Costa Rica provided financial support.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Briceño, R.D., Eberhard, W.G. (2015). Species-Specific Behavioral Differences in Tsetse Fly Genital Morphology and Probable Cryptic Female Choice. In: Peretti, A., Aisenberg, A. (eds) Cryptic Female Choice in Arthropods. Springer, Cham. https://doi.org/10.1007/978-3-319-17894-3_15
Download citation
DOI: https://doi.org/10.1007/978-3-319-17894-3_15
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-17893-6
Online ISBN: 978-3-319-17894-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)