The evolution and diversity of intra-male sperm translocation in Odonata: a unique behaviour in animals
Behavioural diversity is a basic component of biodiversity, with implications in ecological interactions at the intra- and interspecific levels. The reproductive behaviour of Odonata (dragonflies and damselflies) is unique among insects and conditioned by the anatomical separation between the male’s reproductive organs and the intromittent organ. Prior to mating, males must translocate sperm from the genital pore in the ninth abdominal segment to the seminal vesicle located ventrally in the second abdominal segment. This behaviour, exclusive to odonates, is known as intra-male sperm translocation (ST). Here, we review the literature on ST and use phylogenetic comparative analyses to investigate the evolution of ST within the Odonata. Information on ST was compiled for 176 species, with the commonest variant being ST once per mating, after tandem formation (66%). Other variants found were ST involving precopulatory genital touching (10%), ST by the male alone before tandem (16%) or after copulation (5%), and repetition of ST during the same copulation (3%). The precopulatory genital touching might have evolved to detect female receptivity. ST before tandem formation might be favoured when mating opportunities are scarce and copulations are brief. ST after mating might be favoured if males need to be ready to copulate fast. Finally, repeated ST could have evolved through postcopulatory sexual selection in males with limited sperm removal ability, as a means to improve their sperm competition. The most plausible scenario for the evolution of ST is that the ancestors of the Odonata produced a spermatophore and attached it to the body, leading towards the evolution of the secondary genitalia in males. Our study emphasises the role of behavioural diversity to understand behavioural evolution.
Unique behaviours are exclusive of a few individuals, populations and/or species. The intra-male sperm translocation (ST) of dragonflies and damselflies is a unique behaviour in animals: before mating, males need to transfer sperm from the primary to the secondary genitalia, which are anatomically separated. Thus, the viability and quality of sperm (i.e. fertility) will depend on the timing of ST relative to copulation. Our literature review found a variety of ST variants, being ST in tandem and before copulation the ancestral strategy. We discuss putative evolutionary routes for all the variants found and emphasise the importance of retrieving detailed observations of such unique behaviours in the field, which could help to better understand behavioural evolution in this insect group. Behavioural diversity is rarely addressed by conservation strategies, despite unique behaviours being at a higher risk of extinction.
KeywordsDragonflies Damselflies Reproductive behaviour Ethodiversity
We thank Reiner Ritcher for providing the picture in Fig. 1e and for sharing with us his unpublished observations, Andreas Martens for his help with German literature and Naoya Ishizawa for providing us with pdfs and translations of very relevant Japanese papers. Two anonymous reviewers provided comments that helped us improved our manuscript.
ART is supported by an FPI grant of the Spanish Ministry of Economy and Competitiveness (MINECO, BES-2015-071965). Funding was provided by a grant from MINECO, including FEDER funds to ACR (CGL2014-53140-P).
- Corbet PS (1999) Dragonflies. Behaviour and ecology of Odonata. Harley Books, EssexGoogle Scholar
- Cordero A (1992) Sexual cannibalism in the damselfly species Ischnura graellsii (Odonata: Coenagrionidae). Ent Gen 17:17–20Google Scholar
- Cordero A, Santolamazza-Carbone S, Utzeri C (1992) A twenty-four-hours-lasting tandem in Coenagrion scitulum (Ramb.) in the laboratory (Zygoptera: Coenagrionidae). Notul Odonatol 3:166–167Google Scholar
- Cordero-Rivera A, Andrés JA (2002) Male coercion and convenience polyandry in a Calopterygid damselfly (Odonata). J Insect Sci 2:14Google Scholar
- 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
- Córdoba-Aguilar A, Cordero-Rivera A (2008) Cryptic female choice and sexual conflict. In dragonflies and damselflies. In: Córdoba-Aguilar A (ed) Model organisms for ecological and evolutionary research. Oxford University Press, Oxford, pp 189–202Google Scholar
- Dijkstra KDB, Bechly G, Bybee SM, Dow RA, Dumont HJ, Fleck G, Garrison RW, Hämäläinen M, Kalkman VJ, Karube H, May ML, Orr AG, Paulson D, Rehn AC, Theischinger G, Trueman JWH, van Tol J, von Ellenrieder N, Ware J (2013) The classification and diversity of dragonflies and damselflies (Odonata). In: Zhang ZQ (ed) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness, Zootaxa, vol 3730, p 36-45Google Scholar
- Fincke OM (1984) Giant damselflies in a tropical forest: reproductive biology of Megaloprepus caerulatus with notes on Mecistogaster (Zygoptera: Pseudostigmatidae). Adv Odonatol 2:13–27Google Scholar
- Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, New YorkGoogle Scholar
- Kearse M, Moir R, Wilson A, Stone-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Dummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefGoogle Scholar
- Logan ER (1971) A comparative ecological and behavioral study of two species of damselflies, Enallagma boreale (Selys) and Enallagma carunculatum (Morse) (Odonata: Coenagrionidae). PhD Thesis, Washington State University, Pullman, WashingtonGoogle Scholar
- Lorenzo-Carballa MO, Cordero-Rivera A (2014) Odonates. In: Vargas P, Zardoya R (eds) The tree of life. Sinauer, Sunderland, pp 352–363Google Scholar
- Miller PL, Miller CA (1981) Field observations on copulatory behaviour in Zygoptera, with an examination of the structure and activity of male genitalia. Odonatologica 10:201–218Google Scholar
- Naraoka H (2014) Reproductive behavior of Mortonagrion hirosei Asahina, 1972 in Miyagi prefecture, with special reference to intra-male sperm translocation and copulatory process. Tombo 54:46–50Google Scholar
- Proctor HC (1998) Indirect sperm transfer in arthropods: behavioral and evolutionary trends. J Appl Entomol 43:153–174Google Scholar
- Rambaut A, Drummond AJ (2014) Tracer v 1.64. Available from: http://beast.bio.ed.ac.uk/Tracer
- Robertson HM, Tennessen KJ (1984) Precopulatory genital contact in some Zygoptera. Odonatologica 13:591–595Google Scholar
- Utzeri C, Ottolenghi C (1992) Further observations on intra-male sperm translocation behaviour in Anisoptera. Notul Odonatol 3:145–149Google Scholar
- Weygoldt P (1969) The biology of Pseudoscorpions. Harvard University Press, CambridgeGoogle Scholar