Does Large Body Size in Males Facilitate Coercive Mating? A Study in Propylea dissecta Mulsant (Coleoptera: Coccinellidae)
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Abstract
Coercive mating, where males force copulation despite female resistance, is a common reproductive
strategy in many species. But there is no such studies on Ladybirds so far. The current study aims
to examine how male body size influences coercive mating and its subsequent effects on female
reproductive success in Propylea dissecta. Specifically, the study tests the hypotheses that smaller males are more likely to engage in coercive mating, that females mated by smaller males will take
longer to initiate second matings, and that fecundity will be reduced in females mated by smaller
males due to the energy expended in resisting harassment. In this experiment, young female beetles
were paired with either large or small males in no-choice mating combinations. After the first mating,
females were allowed to remate with either a large or small male, and mating behaviour, reproductive
parameters (fecundity and egg viability), and offspring development were recorded. The results
indicated that females paired with smaller males took longer time to commence both first and second
matings, and their fecundity was significantly reduced, though egg viability was unaffected. The
findings suggest that coercive mating is more costly for females, with smaller males being more
persistent in their attempts to mate, despite being less competitive in size. Larger males, on the other
hand, demonstrated a clear advantage in coercive mating scenarios, as females paired with them
commenced mating significantly faster and exhibited higher fecundity compared to those paired with
smaller males. This study highlights the significance of male body size in shaping mating dynamics
and sexual selection in ladybird beetles.
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References
Alcock, J. (2009). Animal behavior. Sinauer Associates: Sunderland, p 535.Allen, G.R. and Simmons, L.W. (1996). Coercive mating, fluctuating asymmetry and male mating success in the dung fly Sepsis cynipsea. Animal Behaviour, 52: 737-741.
Allen, J.J., Akkaynak, D., Schnell, A.K. and Hanlon, R.T. (2017). Dramatic fighting by male cuttlefish for a female mate. The American Naturalist, 190(1): 144-151.
Ancco Valdivia, F.G., Alves-Silva, E. and Del‐Claro, K. (2020). Differences in size and energy content affect the territorial status and mating success of a neotropical dragonfly. Austral Ecology, 45(6):748-758.
Andersson, M. (1994). Sexual Selection. Princeton University Press: Princeton, NJ.
Arnqvist, G. and Nilsson, T. (2000). The evolution of polyandry multiple mating and female fitness in insects. Animal Behaviour, 60: 145–164.
Arnqvist, G. and Rowe, L. (1995). Sexual conflict and arms races between the sexes – a morphological adaptation for control of mating in a female insect. Proceedings of the Royal Society of London B:Biological Sciences, 261: 123–127.
Arnqvist, G. and Rowe, L. (2005a). Sexual Conflict. Princeton University Press: Princeton, NJ.
Arnqvist, G. and Rowe, L. (2005b). Sexual conflict prior to mating. In: Sexual conflict (Eds. Arnqvist, G. and Rowe, L.). Princeton University Press. Pp. 44–91.
Bertram, M.G., Saaristo, M., Baumgartner, J.B., Johnstone, C.P., Allinson, M., Allinson, G. and Wong, B.B. (2015). Sex in troubled waters: widespread agricultural contaminant disrupts reproductive behaviour in fish. Hormones and Behavior, 70: 85-91.
Beukeboom, L.W. (2018). Size matters in insects–an introduction. EntomologiaExperimentalis et Applicata, 166(1): 2-3.
Biaggio, M.D., Sandomirsky, I., Lubin, Y., Harari, A.R. and Andrade, M.C. (2016). Copulation withimmature females increases male fitness in cannibalistic widow spiders. Biology Letters, 12(9):20160516.
Bista, M. and Omkar (2013). Effects of body size and prey quality on the reproductive attributes of twoaphidophagous Coccinellidae (Coleoptera) species. The Canadian Entomologist, 145: 566–576.
Blanckenhorn, W.U., Hosken, D.J., Martin, O.Y., Reim, C., Teuschl, Y. and Ward, P.I. (2002). The costsof copulating in the dung fly Sepsis cynipsea. Behavioral Ecology, 13(3): 353-358.
Bownes, M. and Partridge, L. (1987). Transfer of molecules from ejaculate to females in Drosophila melanogaster and Drosophila pseudoobscura. Journal of Insect Physiology, 33(12): 941-947.
Brennan, P.L. and Prum, R.O. (2012). The limits of sexual conflict in the narrow sense: new insights fromwaterfowl biology. Philosophical Transactions of the Royal Society B: Biological Sciences, 367(1600): 2324-2338.
Bretman, A., Westmancoat, J.D. and Chapman, T. (2013). Male control of mating duration followingexposure to rivals in fruitflies. Journal of Insect Physiology, 59(8): 824-827.
Carbone, S.S. and Rivera, A.C. (1998). Sperm competition, cryptic female choice and prolonged mating inthe eucalyptus snout-beetle, Gonipterus scutellatus (Coleoptera, Curculionidae). Etologia, 6: 33–40.
Chapman, T., Arnqvist, G., Bangham, J. and Rowe, L. (2003). Sexual conflict. Trends in Ecology & Evolution, 18(1): 41–47.
Charlesworth, B. (1987). The heritability of fitness. In: Sexual Selection: Testing the Alternatives (Eds.Bradbury, J.W. and Andersson, M.B.). Wiley: Chichester, UK. Pp.21-40.
Cheng, K.M., Burns, J.T. and McKinney, F. (1983). Forced copulation in captive mallards: III. Sperm competition. The Auk, 100: 302–10.
Chesser, R.K., and Baker, R.J. (1996). Effective sizes and dynamics of uniparentally and diparentally inherited genes. Genetics, 144: 1225–1235.
Clutton-Brock, T.H. and Parker, G.A. (1995). Sexual coercion in animal societies. Animal Behaviour, 49(5): 1345-1365
Conroy, L.P. and Gray, D.A. (2014). Forced copulation as a conditional alternative strategy in camel crickets. Behavioral Ecology and Sociobiology, 68(9): 1431-1439.
Cooper, M.A. and Bernstein, I.S. (2000). Social grooming in Assamese macaques (Macaca assamensis). American Journal of Primatology, 50: 77–85.
Cordero, A. and Andrés, J.A. (2002). Male coercion and convenience polyandry in a calopterygid damselfly. Journal of Insect Science, 2(1): 14.
Cordero, C. and Eberhard, W.G. (2003). Female choice of sexually antagonistic male adaptations: a critical review of some current research. Journal of Evolutionary Biology, 16: 1–6.
Cordero, A. (1999). Forced copulations and female contact guarding at a high male density in a calopterygid damselfly. Journal of Insect Behavior, 12(1): 27-37.
Crean, C.S., Dunn, D.W., Day, T.H. and Gilburn, A.S. (2000). Female mate choice for large males in several species of seaweed fly (Diptera: Coelopidae). Animal Behaviour, 59(1): 121-126.
Crudgington, H.S. and Siva-Jothy, M.T. (2000). Genital damage, kicking and early death. Nature, 407: 855-856.
Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. Murray: London.
Dawkins, R. (1980). Good strategy or evolutionarily stable strategy? In: Sociobiology: Beyond nature /nurture? (Eds. Barlow, G.W. and Silverberg, J.). Westview Press: Boulder, Colorado. Pp. 331-367.
De Luca, P.A. and Cocroft, R.B. (2008). The effects of age and relatedness on mating patterns in thornbug treehoppers: inbreeding avoidance or inbreeding tolerance? Behavioral Ecology andSociobiology, 62(12): 1869-1875.
Deb, R., Bhattacharya, M. and Balakrishnan, R. (2012). Females of a tree cricket prefer larger males but not the lower frequency male calls that indicate large body size. Animal Behaviour, 84(1): 137-149.
Dukas, R. and Jongsma, K. (2012). Costs to females and benefits to males from forced copulations in fruit flies. Animal Behaviour, 84(5): 1177-1182.
Eberhard, W.G. (2002). The function of female resistance behavior: intromission by male coercion vs female cooperation in sepsidflies (Diptera: Sepsidae). Revista de Biologia Tropical, 50: 485–505.
Fu, Y., Cai, C., Chen, P., Xuan, Q., Myint, T. A., & Huang, D. (2024). Group mating in Cretaceous water striders. Proceedings of the Royal Society B, 291(2020), 20232546.
Fukaya, M. (2004). Effects of male body size on mating activity andfemale mate refusal in the yellow-spotted longicorn beetle, Psacotheahilaris (Pascoe) (Coleoptera: Cerambycidae):Are smallmales inferior in mating? Applied Entomology and Zoology, 39:603–609
Ghiselin, M.T. (1974). The Economy of Nature and the Evolution of Sex. University of California Press: Berkeley, CA.
Gibson, K.N., Vick, L.G., Palma, A.C., Carrasco, F.M., Taub, D. and Ramos‐Fernández, G. (2008). Intracommunity infanticide and forced copulation in spider monkeys: a multi‐site comparison between Cocha Cashu, Peru and Punta Laguna, Mexico. American Journal of Primatology: Official Journalof the American Society of Primatologists, 70(5): 485-489.
Gotthard K., Berger D. and Walters R. (2007). What keeps insects small? Time limitation during oviposition reduces the fecundity benefit of female size in a butterfly. The American Naturalist, 169: 768-779.
Gowaty, P.A. (1997). Sexual dialectics, sexual selection, and variation in reproductive behavior. In Feminism and Evolutionary Biology. Springer: Boston, MA. Pp. 351-384.
Haddrill, P.R., Shuker, D.M., Amos, W., Majerus, M.E. and Mayes, S. (2008). Female multiple mating in wild and laboratory populations of the two‐spot ladybird, Adalia bipunctata. MolecularEcology, 17(13): 3189-3197.
Harano, T. (2015). Receptive females mitigate costs of sexual confict. Journal of Evolutionary Biology, 28:320–327.
Head, M.L. and Brooks, R. (2006). Sexual coercion and the opportunity for sexual selection in guppies. Animal behaviour, 71(3): 515-522.
Hemptinne, J.L., Lognay, G. and Dixon, A.F.G. (1998). Mate recognition in the two-spot ladybird beetle, Adalia bipunctata: role of chemical and behavioural cues. Journal of Insect Physiology, 44(12): 1163-1171.
Hettyey, A., Vagi, B., Hevizi, G. and Toeroek, J. (2009a). Changes in sperm stores, ejaculate size, fertilization success, and sexual motivation over repeated matings in the common toad, Bufo bufo (Anura: Bufonidae). Biological Journal of the Linnean Society, 96(2): 361-371.
Hodek, I. and Ceryngier, P. (2000). Sexual activity in Coccinellidae (Coleoptera): a review. European Journal of Entomology, 97: 449-456.
Honek, A. (1993). Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos, 66: 483–492.
Iwasa, Y., Pomiankowski, A. and Nee, S. (1991). The evolution of costly mate preferences II. The handicap‖ principle. Evolution, 45(6): 1431-1442.
Kaufmann, T. (1996). Dynamics of sperm transfer, mixing, and fertilization in Cryptolaemus montrouzieri(Coleoptera: Coccinellidae) in Kenya. Annals of the Entomological Society of America, 89(2): 238-242.
Khan, M. K. (2020). Female pre-reproductive coloration reduces matingharassment in damselfies. Evolution, 74:2293–2303.
Killian, K.A., Snell, L.C., Ammarell, R. and Crist, T.O. (2006). Suppression of escape behaviour during mating in the cricket Acheta domesticus. Animal Behaviour, 72: 487–502.
Kokko, H., Jennions, M.D. and Brooks, R. (2006). Unifying and testing models of sexual selection. Annual Review of Ecology, Evolution, and Systematics, 37: 43-66.
Lauer, M.J., Sih, A. and Krupa, J.J. (1996). Male density, female density and inter-sexual conflict in a stream-dwelling insect. Animal Behaviour, 52(5): 929-939.
Majerus, M.E.N. (1994a). Ladybirds. Harper Collins, London.
Manning, A. (1967). The control of sexual receptivity in female Drosophila. Animal Behaviour, 15: 239-250.
Markow, T.A. (2000). Forced matings in natural populations of Drosophila. The American Naturalist, 156(1): 100-103.
McLain, D.K. and Pratt, A.E. (1999). The cost of sexual coercion and heterospecific sexual harassment on the fecundity of a host-specific, seed-eating insect (Neacoryphusbicrucis). Behavioral Ecology andSociobiology, 46(3): 164-170
Mineau, P., McKinney, F. and Derrickson, S. R. (1983). Forced copulation in waterfowl. Behaviour, 86(3- 4): 250-293.
Moshitzky, P., Fleischmann, I., Chaimov, N., Saudan, P., Klauser, S., Kubli, E. and Applebaum, S.W. (1996). Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Archives of Insect Biochemistry and Physiology, 32: 363-374.
Muller, M.N., Kahlenberg, S.M. and Wrangham, R.W. (2009). Male aggression and sexual coercion of females in primates. In: Sexual Coercion in Primates and Humans (Eds. Muller, M.N. and Wrangham, R.W.). Harvard University Press: Cambridge, MA.
Obara, Y., Fukano, Y., Watanabe, K., Ozawa, G.and Sasaki, K. (2011). Serotonininduced mate rejection in the female cabbage butterfy, Pieris rapaecrucivora.Naturwissenschaften 98:989–993.
Obata, S. and Hidaka, T. (1987). Ejection and ingestion of the spermatophore by the female ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). The Canadian Entomologist, 119(6): 603-604.
Obata, S. (1987). Mating behaviour and sperm transfer in ladybeetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Applied Entomology and Zoology, 22: 434–442.
Obata, S. (1988). Mating refusal and its significance in female of the ladybird beetle, Harmonia axyridis. Journal of Physiological Entomology, 13: 193-199.
Oberhauser, K.S. (1988). Male monarch butterfly spermatophore mass and mating strategies. Animal Behaviour, 36: 1384-1388.
Omkar and James, B.E. (2005). Reproductive behaviour of an aphidophagous ladybeetle, Coccinella transversalis (Coleoptera: Coccinellidae). International Journal of Tropical Insect Science, 25: 96–102.
Omkar and Mishra G. (2005). Mating in aphidophagous ladybirds: costs and benefits. Journal of Applied Entomology, 129(8): 432-436.
Omkar and Mishra, G. (2009). Optimization of age difference between mates maximizes reproductive output. BioControl, 54(5): 637-650.
Omkar and Pervez, A. (2000a). Biodiversity of predaceous coccinellids (Coleoptera: Coccinellidae) in India: A review. Journal of Aphidology, 14: 41-66.
Omkar and Pervez, A. (2000b). Sexual dimorphism in Propylea dissecta (Mulsant), (Coccinellidae: Coleoptera). Journal of Aphidology, 14: 139-140.
Omkar and Pervez, A. (2005). Mating behavior of an aphidophagous ladybird beetle, Propylea dissecta (Mulsant). Insect Science, 12(1): 37-44.
Omkar and Singh, S.K. (2010). Mating behaviour of the aphidophagous ladybird beetle Coelophorasaucia(Coleoptera: Coccinellidae). International Journal of Tropical Insect Science, 30(1): 3-10.
Omkar and Srivastava, S. (2002). Reproductive behaviour of an aphidophagous ladybeetle, Coccinella septempunctata Linnaeus. European Journal of Entomology, 99: 465-470.
Peretti, A.V. and Aisenberg, A. (2011). Communication under sexual selection hypotheses: challenging prospects for future studies under extreme sexual conflict. Acta Ethologica, 14(2): 109-116
Perry, J.C. and Rowe, L. (2010). Condition-dependent ejaculate size and composition in a ladybird beetle. Proceedings of the Royal Society B: Biological Sciences, 277(1700): 3639-3647
Pervez, A., Omkar and Richmond, A.S. (2004). The influence of age on reproductive performance of the predatory ladybird beetle, Propylea dissecta. Journal of Insect Science, 4: 1-8.
Pilastro, A., Benetton, S. and Bisazza, A. (2003). Female aggregation and male competition reduce costs of sexual harassment in the mosquitofish Gambusia holbrooki. Animal Behaviour, 65(6): 1161-1167.
Pitnick, S. and Markow, T.A. (1994). Male gametic strategies: sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pacheaand its relatives. TheAmerican Naturalist, 143(5): 785-819.
Ransford M.O. (1997). Sperm competition in the 2-spot ladybird, Adalia bipunctata. Ph.D. thesis, University of Cambridge.
Ravi Ram, K. and Wolfner, M.F. (2007). Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integrative and Comparative Biology, 47(3): 427- 445.
Savalli, U.M. and Fox, C.W. (1998). Sexual selection and the fitness consequences of male body size in the seed beetle Stator limbatus. Animal Behaviour, 55(2): 473-483.
Seeley, C. and Dukas, R. (2011). Teneral matings in fruit flies: male coercion and female response. Animal Behaviour, 81(3): 595-601.
Seeley, C.J. (2010). An Investigation of Teneral Matings, Male Coercion, and Female Response. A Second Investigation of Caffeine Tolerance in Drosophila Melanogaster (Doctoral dissertation).
Shahid, M., Siddiqui, A., Omkar and Mishra, G. (2016). Mating alters the rate of development of ovarioles in the ladybird, Propylea dissecta (Coleoptera: Coccinellidae). European Journal of Entomology, 113: 44-50.
Shine, R. and Mason, R.T. (2005). Does large body size in males evolve to facilitate forcible insemination? A study on garter snakes. Evolution, 59: 2426–2432.
Silk, P.J., Sweeney, J., Wu, J., Sopow, S., Mayo, P.D. and Magee, D. (2011). Contact sex pheromones identified for two species of longhorned beetles (Coleoptera: Cerambycidae) Tetropiumfuscumand T. cinnamopterumin the subfamily Spondylidinae. Environmental Entomology, 40(3): 714-726.
Smuts, B.B. and Smuts, R.W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior, 22: 1–63.
Solensky, M.J. (2004). The effect of behavior and ecology on male mating success in overwintering monarch butterflies (Danaus plexippus). Journal of Insect Behavior, 17: 723–743.
Tallamy, D.W., Powell, B.E. and McClafferty, J.A. (2002). Male traits under cryptic female choice in the spotted cucumber beetle (Coleoptera: Chrysomelidae). Behavioral Ecology, 13(4): 511-518.
Taylor, M.L., Wedell, N. and Hosken, D.J. (2007). The heritability of attractiveness. Current Biology, 17(22): R959-R960.
Thompson, D.J. and Fincke, O.M. (2002). Body size and fitness in Odonata, stabilising selection and a meta‐analysis too far? Ecological Entomology, 27(3): 378-384.
Thornhill, R. and Palmer, C. (2000). A Natural History of Rape: Biological Bases of Sexual Coercion. MIT Press: Cambridge, Massachusetts.
Thornhill, R. (1984). Alternative female choice tactics in the scorpionflyHylobittacusapicalis(Mecoptera) and their implications. The American Naturalist, 24: 367–383.
Tinzaara, W., Gold, C.S., Dicke, M., Van Huis, A. and Ragama, P.E. (2011). Effect of age, female mating status and density on the banana weevil response to aggregation pheromone. African Crop ScienceJournal, 19: 1021–9730.
Ubukata H. (1984). Oviposition site selection and avoidance of additional mating by females of the dragonfly, CorduliaaneneaamuriensisSelys (Corduliidae). Researches on Population Ecology, 26: 285-301.
Afaq, U. and Omkar (2017). Polygyny influences the fitness of Parthenium beetle, Zygogramma bicolorata Pallister. Journal of Asia-Pacific Entomology, 20(1), 215-219.
Vahed, K. (2002). Coercive copulation in the alpine bushcricketAnonconotus alpinus Yersin (Tettigoniidae: Tettigoniinae: Platycleidini). Ethology, 108(12): 1065-1075.
Waage, J.K. (1987). Choice and utilization of oviposition sites by female Calopteryx maculata (Odonata: Calopterygidae). I. Influence of site size and the presence of other females. Behavioral Ecology andSociobiology, 20: 439-446.
Wallen, M.M., Patterson, E.M., Krzyszczyk, E. and Mann, J. (2016). The ecological costs to females in a system with allied sexual coercion. Animal Behaviour, 115: 227-236.
Wedell, N., Gage, M.J. and Parker, G.A. (2002). Sperm competition, male prudence and sperm-limited females. Trends in Ecology and Evolution, 17(7): 313-320.
Yadav, A. Wang, Q. and He, X.Z. (2010). Effect of body weight on reproductive performance of Micromustasmaniae(Walker) (Neuroptera: Hemerobiidae). Insect Biology, 63: 208–213.
Yan, J. L., Dobbin, M. L., & Dukas, R. (2024). Sexual conflict and sexual networks in bed bugs: the fitness cost of traumatic insemination, female avoidance and male mate choice. Proceedings of the Royal Society of London. Series B: BiologicalSciences, 291(2027), 20232808.
Yasui, Y. (1994). Adaptive control of copulation duration by males under sperm competition in the mite, Macrochelesmuscaedomesticae. Experimental & Applied Acarology, 18(9): 543-554.
Zeh, J.A. and Zeh, D.W. (2003). Toward a new sexual selection paradigm: Polyandry, conflict and incompatibility (Invited article). Ethology, 109(12): 929-950.
Zeh, J.A. and Zeh, D.W. (1997). The evolution of polyandry II: post–copulatory defenses against genetic incompatibility. Proceedings of the Royal Society of London. Series B: BiologicalSciences, 264(1378): 69-75.