Abstract
Male abdominal grasping apparatus that are used to secure a female prior, during and after mating, are widespread in arthropods. The scarce evidence regarding its selective regime suggests that they are male adaptations to circumvent female mating decisions, as predicted by the sexual conflict hypothesis. A recent discussion regarding this way of selection suggests that, similar to weapons and traits that have to do with physical endurance, grasping apparatus should show hyperallometry (proportionally larger compared to body size) as an indication of selection towards increased size. We have tested this idea by measuring the length, width and area of the grasping apparatus of five dragonfly species (Anax junius, Rhionaeschna multicolor, Dythemis nigrescens, D. sterilis and Phyllogomphoides pacificus). We used two proxies of body size (wing and body length). Our measures did not indicate any pattern of hyperallometry. Thus, the grasping apparatus in these animals does not seem to be positively selected for increased size as would be expected if they were forcing females to mate. Given this, we discuss three other explanations for the maintenance of the grasping apparatus in odonates: 1) a firm grip that secures the tandem and mating position; 2) courtship devices subject to female choice; and, 3) isolation structures that mechanically prevent interspecific matings. The first hypothesis, however, could not explain the highly elaborated and species specific morphology of grasping apparatus in these animals. Support for the second hypothesis comes from the fact that odonate females have mechanoreceptor sensilla embedded in their mesostigmal plates (the place grabbed by the grasping apparatus). For the third hypothesis, coevolutionary patterns in morphology in the grasping apparatus and mesostigmal plates in some Zygoptera can also be used as support.
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References
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 146–163. doi:10.1017/CBO9780511721946.009
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton
Cham S (2008) Underwater tandem formation in common blue damselfly Enallagma cyathigerum and the need for contact guarding. J Br Dragonfly Soc 24:24–31
Clutton-Brock TH (1982) The functions of antlers. Behaviour 79:108–124. doi:10.1163/156853982X00201
Corbet PS (1999) Dragonflies: behaviour and ecology of Odonata. Harley, Essex
Cordero A (1999) Forced copulations and female contact guarding at a high male density in a Calopterygid damselfly. J Insect Behav 12:27–37. doi:10.1023/a:1020972913683
Cordero Rivera A, Andres JA (2002) Male coercion and convenience polyandry in a calopterygid damselfly. J Insect Sci 2:1–7 http://insectscience.org/2.14
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 characters in animals. Oxford University Press, Oxford, pp 332–352
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 3:166–167
Cordero A, Santolamazza-Carbone S, Utzeri C (1995) Male disturbance, repeated insemination and sperm competition in the damselfly Coenagrion scitulum (Zygoptera: Coenagrionidae). Anim Behav 49:437–449. doi:10.1006/anbe.1995.0057
Córdoba-Aguilar A (2006) Sperm ejection as a possible cryptic female choice mechanism in Odonata (Insecta). Physiol Entomol 31:146–153. doi:10.1111/j.1365-3032.2005.00498.x
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. doi:10.1603/008.102.0414
Córdoba-Aguilar A, López-Valenzuela A, Brunel O (2010) Allometry in damselfly ornamental and genital traits: solving some pitfalls of allometry and sexual selection. Genetica 138:1141–1146. doi:10.1007/s10709-010-9504-6
Cothran RD (2008) Phenotypic manipulation reveals sexual conflict over precopula duration. Behav Ecol Sociobiol 62:1409–1416. doi:10.1007/s00265-008-0570-z
Dunkle SW (1984) Head damage due to mating in Ophiogomphus dragonflies (Anisoptera: Gomphidae). Not Odonatol 2:63–64
Dunkle SW (1991) Aeolagrion axine spec. nov., a new damselfly from Ecuador (Zygoptera: Coenagrionidae). Odonatologica 20:239–244
Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Harvard
Eberhard WG (2009) Static allometry and animal genitalia. Evolution 63:48–66. doi:10.1111/j.1558-5646.2008.00528.x
Eberhard WG (2010) Rapid divergent evolution of genitalia: theory and data updated. In: Leonard JL, Córdoba-Aguilar A (eds) The evolution of primary sexual characters in animals. Oxford University Press, Oxford, pp 40–78
Eberhard W, Huber B, Rodriguez R et al (1998) One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution 52:415–431. doi:10.2307/2411078
Fincke OM (1984) Giant damselflies in a tropical forest: reproductive biology of Megaloprepus coerulatus with notes on Mecistogaster (Zygoptera: Pseudostigmatidae). Adv Odonatol 2:13–27
Gao Q, Hua B (2013) Co-evolution of the mating position and male genitalia in insects: a case study of a hangingfly. PLoS One 8(12):e80651. doi:10.137/journal.pone.0080651
Gorb SN (1998a) Functional morphology of the head-arrester system in Odonata. Zoologica 148:1–132. doi:10.1016/S0022-1910(98)00068-7
Gorb SN (1998b) Origin and pathway of the epidermal secretion in the damselfly head- arresting system (Insecta: Odonata). J Insect Physiol 44:1053–1061
Gorb SN (1999) Evolution of the dragonfly head-arresting system. Proc R Soc B Biol Sci 266:525–535. doi:10.1098/rspb.1999.0668
Green A (1992) Positive allometry is likely with mate choice, competitive display and other functions. Anim Behav 43:170–172. doi:10.1016/s0003-3472(05)80086-7
Huber BA (2010) Mating positions and the evolution of asymmetric insect genitalia. Genetica 138:19–25. doi:10.1007/s10709-008-9339-6
Khila A, Abouheif E, Rowe L (2012) Function, developmental genetics, and fitness consequences of a sexually antagonistic trait. Science 336:585–589. doi:10.1126/science.1217258
Kodrick-Brown A, Sibly RM, Brown JH (2006) The allometry of ornaments and weapons. Proc Natl Acad Sci U S A 103:8733–8738. doi:10.1073/pnas.0602994103
Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam
McPeek MA, Shen L, Torrey JZ, Farid H (2008) The tempo and mode of three-dimensional morphological evolution in male reproductive structures. Am Nat 171:E158–E178. doi:10.1086/587076
McPeek MA, Shen L, Farid H (2009) The correlated evolution of three-dimensional reproductive structures between male and female damselflies. Evolution 63:73–83. doi:10.1111/j.1558-5646.2008.00527.x
McPeek MA, Symes LB, Zong DM, McPeek CL (2011) Species recognition and patterns of population variation in the reproductive structures of a damselfly genus. Evolution 65:419–428. doi:10.1111/j.1558-5646.2010.01138.x
Meurgey F, Faucheux MJ (2009) Sensilla on the male paraprocts of Protoneura romanae Meurgey (Zygoptera: Protoneuridae). Odonatologica 38:267–271
Outomuro D, Cordero-Rivera A (2012) Allometry of secondary, primary, and nonsexual traits in the beautiful demoiselle (Calopteryx virgo meridionalis). Can J Zool 90:1094–1101. doi:10.1139/z2012-076
Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos Trans R Soc Lond B Biol Sci 361:235–259. doi:10.1098/rstb.2005.1785
Paulson D (1974) Reproductive isolation in damselflies. Syst Zool 23:40–49. doi:10.2307/2412238
Peretti A, Eberhard WG, Briceño RD (2006) Copulatory dialogue: female spiders sing during copulation to influence male genitalic movements. Anim Behav 72:413–421. doi:10.1016/j.anbehav.2006.01.014
Perry JC, Rowe L (2012) Sexual conflict and antagonistic coevolution across water strider populations. Evolution 66:544–557. doi:10.1111/j.1558-5646.2011.01464.x
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Core Development Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Robertson H, Paterson H (1982) Mate recognition and mechanical isolation in Enallagma-damselflies (Odonata, Coenagrionidae). Evolution 36:243–250. doi:10.2307/2408042
Rodríguez-Márquez IA, Peretti AV (2010) Intersexual cooperation during male clasping of external female genitalia in the spider Physocyclus dugesi (Araneae, Pholcidae). J Ethol 28:153–163. doi:10.1007/s10164-009-0168-6
Rowe L, Arnqvist G (2002) Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes. Evolution 56:754–767. http://www.jstor.org/stable/3061658 doi: 10.1111/j.0014-3820.2002.tb01386.x
Sánchez-Guillén RA, Wullenreuther M, Cordero Rivera A (2012) Strong asymmetry in the relative strengths of prezygotic and postzygotic barriers between two damselfly sister species. Evolution 66:690–707. doi:10.1111/j.1558-5646.2011.01469.x
Svensson EI, Karlsson K, Friberg M, Eroukhmanoff F (2007) Gender differences in species recognition and the evolution of asymmetric sexual isolation. Curr Biol 17:1943–1947. doi:10.1016/j.cub.2007.09.038
Waage JK (1979) Reproductive character displacement in Calopteryx (Odonata: Calopterygidae). Evolution 33:104–116. doi:10.2307/2407369
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291. doi:10.1017/S1464793106007007
Wildermuth H (1984) Drei aussergewohnliche Beobachtungen zum Fortpflanzungsverhalten der Libellen. Mitteilungen der Entomol Gesellschaft Basel 34:121–129
Wildermuth H (1991) Behaviour of Perithemis mooma Kirby at the oviposition site (Anisoptera: Libellulidae). Odonatologica 20:471–478
Acknowledgments
To R. I. Martínez Becerril for his logistic help. Financial support was possible via a PAPIIT-UNAM grant (IN 222312). To one anonymous reviewer whose comments improved a preliminary version.
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Suppl. mat. Figure 1
Male upper grasping apparatus for each species used in this study. Left: distal abdomen with both grasping apparatus; right: the right apparatus used. The right grasping apparatus shows where width (yellow line), area (red line) and length (the most extreme points from basis to distal site) were measured (GIF 128 kb)
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Córdoba-Aguilar, A., Vrech, D.E., Rivas, M. et al. Allometry of Male Grasping Apparatus in Odonates Does Not Suggest Physical Coercion of Females. J Insect Behav 28, 15–25 (2015). https://doi.org/10.1007/s10905-014-9477-x
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DOI: https://doi.org/10.1007/s10905-014-9477-x