Advertisement

The evolution and diversity of intra-male sperm translocation in Odonata: a unique behaviour in animals

  • A. Rivas-TorresEmail author
  • D. Outomuro
  • M. O. Lorenzo-Carballa
  • A. Cordero-Rivera
Original Article

Abstract

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.

Significance statement

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.

Keywords

Dragonflies Damselflies Reproductive behaviour Ethodiversity 

Notes

Acknowledgements

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.

Funding information

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).

Supplementary material

265_2019_2660_MOESM1_ESM.xlsx (42 kb)
ESM 1 (XLSX 42 kb)
265_2019_2660_MOESM2_ESM.docx (577 kb)
ESM 2 (DOCX 576 kb)

References

  1. Bechly G, Brauckmann C, Zessin W, Gröning E (2001) New results concerning the morphology of the most ancient dragonflies (Insecta: Odonatoptera) from the Namurian of Hagen-Vorhalle (Germany). J Zool Syst Evol Res 39:209–226CrossRefGoogle Scholar
  2. Berger-Tal O, Saltz D (2016) Conservation behavior: applying behavioral ecology to wildlife conservation and management. Cambridge University Press, New YorkCrossRefGoogle Scholar
  3. Bouckaert RR, Drummond AJ (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evol Biol 17:42.  https://doi.org/10.1186/s12862-017-0890-6 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Comp Biol 10:1–6CrossRefGoogle Scholar
  5. Caro T, Sherman PW (2012) Vanishing behaviors. Cons Lett 5:159–166CrossRefGoogle Scholar
  6. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47CrossRefGoogle Scholar
  7. Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell E, Sayers W (2016) GenBank. Nucleic Acids Res 44:D67–D72CrossRefGoogle Scholar
  8. Corbet PS (1999) Dragonflies. Behaviour and ecology of Odonata. Harley Books, EssexGoogle Scholar
  9. Cordero A (1992) Sexual cannibalism in the damselfly species Ischnura graellsii (Odonata: Coenagrionidae). Ent Gen 17:17–20Google Scholar
  10. 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
  11. Cordero A, Santolamazza-Carbone S, Utzeri C (1995) Male disturbance, repeated insemination and sperm competition in the damselfly Coenagrion scitulum (Zygoptera: Coenagrionidae). Anim Behav 49:437–449CrossRefGoogle Scholar
  12. Cordero A, Santolamazza-Carbone S, Utzeri C (1998) Mating opportunities and mating costs are reduced in androchrome female damselflies, Ischnura elegans (Odonata). Anim Behav 55:185–197CrossRefGoogle Scholar
  13. Cordero-Rivera A (2016) Sperm removal during copulation confirmed in the oldest extant damselfly, Hemiphlebia mirabilis. PeerJ 4:e2077CrossRefGoogle Scholar
  14. Cordero-Rivera A (2017a) Behavioral diversity (Ethodiversity): a neglected level in the study of biodiversity. Front Ecol Evol 5:1–7CrossRefGoogle Scholar
  15. 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
  16. Cordero-Rivera A, Andrés JA (2002) Male coercion and convenience polyandry in a Calopterygid damselfly (Odonata). J Insect Sci 2:14Google Scholar
  17. 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
  18. 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 41:161–174.  https://doi.org/10.32800/abc.2018.41.0161 CrossRefGoogle Scholar
  19. 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
  20. Córdoba-Aguilar A, González-Tokman D, González-Santoyo I (2018) Insect behaviour. Oxford University Press, OxfordCrossRefGoogle Scholar
  21. 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
  22. Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc B Biol Sci 271:847–852CrossRefGoogle Scholar
  23. Downes JA (1969) The swarming and mating flight of Diptera. Annu Rev Entomol 14:271–298CrossRefGoogle Scholar
  24. 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
  25. 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
  26. Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131CrossRefGoogle Scholar
  27. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, New YorkGoogle Scholar
  28. Ibáñez CM, Keyl F (2010) Cannibalism in cephalopods. Rev Fish Biol Fish 20:123–136CrossRefGoogle Scholar
  29. 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
  30. Li D, Oh J, Kralj-Fiser S, Kuntner M (2012) Remote copulation: male adaptation to female cannibalism. Biol Lett 8:512–515CrossRefGoogle Scholar
  31. 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
  32. Lorenzo-Carballa MO, Cordero-Rivera A (2014) Odonates. In: Vargas P, Zardoya R (eds) The tree of life. Sinauer, Sunderland, pp 352–363Google Scholar
  33. 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
  34. 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
  35. Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Philos Trans R Soc Lond Ser B Biol Sci 255:37–45CrossRefGoogle Scholar
  36. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290CrossRefGoogle Scholar
  37. Pérez-Méndez N, Jordano P, García C, Valido A (2016) The signatures of Anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci Rep 6:24820CrossRefGoogle Scholar
  38. Proctor HC (1998) Indirect sperm transfer in arthropods: behavioral and evolutionary trends. J Appl Entomol 43:153–174Google Scholar
  39. Pupko T, Pe I, Shamir R, Graur D (2000) A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol Biol Evol 17:890–896CrossRefGoogle Scholar
  40. Rambaut A, Drummond AJ (2014) Tracer v 1.64. Available from: http://beast.bio.ed.ac.uk/Tracer
  41. Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223CrossRefGoogle Scholar
  42. Robertson HM (1985) Female dimorphisms and mating behaviour in a damselfly, Ischnura ramburii: females mimicking males. Anim Behav 33:805–809CrossRefGoogle Scholar
  43. Robertson HM, Tennessen KJ (1984) Precopulatory genital contact in some Zygoptera. Odonatologica 13:591–595Google Scholar
  44. Robey C (1975) Observations on breeding behavior of Pachydiplax longipennis (Odonata: Libellulidae). Psyche 82:89–96CrossRefGoogle Scholar
  45. Sanmartín-Villar I, Cordero-Rivera A (2016) Female colour polymorphism and unique reproductive behaviour in Polythore damselflies (Zygoptera: Polythoridae). Neotrop Entomol 45:658–664CrossRefGoogle Scholar
  46. Schneider JM (2014) Sexual cannibalism as a manifestation of sexual conflict. Cold Spring Harb Perspect Biol 6:1–16CrossRefGoogle Scholar
  47. Shuker DM, Simmons LW (2014) The evolution of insect mating systems. Oxford University Press, OxfordCrossRefGoogle Scholar
  48. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  49. Torres-Cambas Y, Cordero-Rivera A (2011) Limited spermathecal sperm removal ability in the damselfly Hypolestes trinitatis (Gundlach) (Odonata: Megapodagrionidae). Int J Odonatol 14:321–328CrossRefGoogle Scholar
  50. Utzeri C, Ottolenghi C (1992) Further observations on intra-male sperm translocation behaviour in Anisoptera. Notul Odonatol 3:145–149Google Scholar
  51. Weygoldt P (1969) The biology of Pseudoscorpions. Harvard University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.ECOEVO LabUniversidade de Vigo, Escola de Enxeñaría ForestalPontevedraSpain
  2. 2.Department of Biological SciencesUniversity of CincinnatiCincinnatiUSA

Personalised recommendations