Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T16:05:06.223Z Has data issue: false hasContentIssue false
  • English
  • Français

Operational sex ratio and paternal age sway mating and reproductive performance in Menochilus sexmaculatus (Coleoptera: Coccinellidae)

Published online by Cambridge University Press:  20 March 2020

Swati Saxena Open the ORCID record for Swati Saxena [Opens in a new window] ,
Geetanjali Mishra Open the ORCID record for Geetanjali Mishra [Opens in a new window]  and
Omkar Open the ORCID record for Omkar [Opens in a new window]
Swati Saxena
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow226007, India
Geetanjali Mishra
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow226007, India
Omkar*
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow226007, India
*
*Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Operational sex ratio and paternal age are known to independently affect mating behaviour and reproductive performance. We conducted experiments to assess the effects of operational sex ratio and paternal age on mating, reproduction, and total development duration of Menochilus sexmaculatus (Fabricius) (Coleoptera: Coccinellidae). Three male-biased sex ratios, no (1:1), modest (1:2), and extreme (1:5) competition treatments, were formed using young, middle-aged, and old males. The reproductive performance of M. sexmaculatus at all ages under extreme competition (1:5) surpassed the other two treatments. More competition among males decreased the time of commencement of mating and increased the duration of copulation. Females laid a greater number of eggs in extreme competition treatments. The operational sex ratio (irrespective of age) had no significant effect on the total developmental duration of offspring. Among different age groups, older males took more time to commence mating and mated for longer durations in all the sex ratio treatments. The number of eggs in the first clutch was lowest when females were mated with older males with increased offspring development duration. Thus, it can be concluded that male-biased sex ratio elevates the performance of M. sexmaculatus. Among different age groups, older males were poor performers than young and middle-aged males.

Type
Research Papers
Information
The Canadian Entomologist , Volume 152 , Issue 3 , June 2020 , pp. 298 - 310
Copyright
© 2020 Entomological Society of Canada

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Subject editor: Chris Starr

References

Abraham, S., Contreres-Navaro, Y., and Perez-Staples, D. 2016. Female age determines re-mating behaviour in wild Mexican fruit flies. Journal of Insect Behavior, 29: 340–354. https://doi.org/10.1007/s10905-016-9562-4.CrossRefGoogle Scholar
Agarwala, B.K. and Yasuda, H. 2000. Competitive ability of ladybird predators of aphids: a review of Cheilomenes sexmaculata (Fabr.) (Coleoptera: Coccinellidae) with a worldwide checklist of preys. Journal of Aphidology, 14: 1–20.Google Scholar
Ahnesjo, I., Kvarnemo, C., and Merilaita, S. 2001. Using potential reproductive rates to predict mating competition among individuals qualified to mate. Behavioral Ecology, 12: 397–401.CrossRefGoogle Scholar
Alonso-Pimentel, H. and Papaj, D.R. 1996. Operational sex ratio versus gender density as determinants of copulation duration in the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Behavioral Ecology and Sociobiology, 39: 171–180.CrossRefGoogle Scholar
Amin, M.R., Bussière, L.F., and Goulson, D. 2012. Effects of male age and size on mating success in the bumble bee Bombus terrestris. Journal of Insect Behavior, 25: 362–374.CrossRefGoogle Scholar
Andersson, M.B. 1994. Sexual selection. Princeton University Press, Princeton, New Jersey, United States of America.CrossRefGoogle Scholar
Bayoumy, M.H. and Michaud, J.P. 2014. Female fertility in Hippodamia convergens (Coleoptera: Coccinellidae) is maximized by polyandry, but reduced by continued male presence. European Journal of Entomology, 111: 513–520.CrossRefGoogle Scholar
Beck, C.W. and Powell, L.A. 2000. Evolution of female mate choice based on male age: are older males better mates? Evolutionary Ecology Research, 2: 107–118.Google Scholar
Beck, C.W. and Promislow, D.E.L. 2007. Evolution of female preference for younger males. Public Library of Science One, 2: e939.Google ScholarPubMed
Berglund, A. 1994. The operational sex-ratio influences choosiness in a pipefish. Behavioral Ecology, 5: 254–258.CrossRefGoogle Scholar
Bista, M. and Omkar, . 2015. Age dependent mate choice influences reproductive and progeny attributes in aphidophagous ladybird beetles (Coleoptera: Coccinellidae). European Journal of Entomology, 112: 648–657.CrossRefGoogle Scholar
Bonduriansky, R.A. and Brassil, C.E. 2002. Rapid and costly ageing in wild male flies. Nature, 420: 377.CrossRefGoogle ScholarPubMed
Bretman, A., Fricke, C., and Chapman, T. 2009. Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness. Proceeding of Royal Society. London B, 276: 1705–1711.CrossRefGoogle ScholarPubMed
Carrillo, J., Danielson-Francois, A., Siemann, E., and Meffert, L. 2012. Male biased sex ratio increases female egg laying and fitness in the housefly, Musca domestica. Journal of Ethology, 30: 247–254.CrossRefGoogle Scholar
Chaudhary, D.D., Mishra, G., and Omkar, . 2015. Prolonged mating in ladybird, Menochilus sexmaculatus: a mate guarding mechanism? Journal of Asia-Pacific Entomology, 18: 453–458.CrossRefGoogle Scholar
Chaudhary, D.D., Mishra, G., and Omkar, . 2017. Strategic mate-guarding behaviour in ladybirds. Ethology, 123: 376–385.CrossRefGoogle Scholar
Clutton-Brock, T.H., Rose, K.E., and Guinness, F.E. 1997. Density related changes in sexual selection in red deer. Proceedings of Royal Society London B, 264: 1509–1516.CrossRefGoogle ScholarPubMed
Clutton-Brock, T.H. and Vincent, A.J. 1991. Sexual selection and the potential reproductive rates of males and females. Nature, 351: 58–60.CrossRefGoogle ScholarPubMed
Cotter, S.C., Ward, R.J.S., and Kilner, R.M. 2010. Age-specific reproductive investment in female burying beetles: independent effects of state and risk of death. Functional Ecology, 25: 652–660.CrossRefGoogle Scholar
Dick, J.T.A. and Elwood, R.W. 1996. Effects of natural variation in sex ratio and habitat structure on mate-guarding decisions in amphipods (Crustacea). Behaviour, 133: 985–996.CrossRefGoogle Scholar
Dixon, A.F.G. and Agarwala, B.K. 2002. Triangular fecundity function and ageing in ladybird beetles. Ecological Entomology, 27: 433–440.CrossRefGoogle Scholar
Dubey, A., Omkar, , and Mishra, G. 2016a. Influence of temperature on reproductive biology and phenotype of a ladybird, Menochilus sexmaculata (Fabricius) (Coleoptera: Coccinellidae). Journal of Thermal Biology, 58: 35–42.CrossRefGoogle Scholar
Dubey, A., Omkar, , and Mishra, G. 2016b. Adult body size drives sexual selection mutually in the ladybirds, Menochilus sexmaculatus. Acta Entomologica Sinica, 59: 209–218.Google Scholar
Emlen, S.T. and Oring, L.W. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197: 215–223.CrossRefGoogle ScholarPubMed
Fedorka, K.M., Winterhalter, W.E., and Ware, B. 2011. Perceived sperm competition intensity influences seminal fluid protein production prior to courtship and mating. Evolution, 65: 584–590.CrossRefGoogle ScholarPubMed
Fox, C.W. 1993. Multiple mating, lifetime fecundity and female mortality of the bruchid beetle, Callosobruchus maculates (Coloeptera: Bruchidae). Functional Ecology, 7: 203–208.CrossRefGoogle Scholar
Friberg, U. and Arnqvist, G. 2003. Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females. Journal of Evolutionary Biology, 16: 797–811.CrossRefGoogle ScholarPubMed
Grant, J.W.A. and Foam, P.E. 2002. Effect of operational sex ratio on female–female versus male–male competitive aggression. Canadian Journal of Zoology, 80: 2242–2246.CrossRefGoogle Scholar
Halliday, T.R. 1978. Sexual selection and mate choice. In Behavioural ecology: an evolutionary approach. Edited by Krebs, J.R. and Davies, N.B.. Blackwell Scientific Publishers, London, United Kingdom. Pp. 180–213.Google Scholar
Halliday, T.R. 1983. The study of mate choice. In Mate choice. Edited by Bateson, P.. Cambridge University Press, Cambridge, United Kingdom. P. 462.Google Scholar
Hansen, T.F. and Price, D.K. 1995. Good genes and old age: do old mates provide superior genes? Journal of Evolutionary Biology, 8: 769–778.CrossRefGoogle Scholar
Head, M.L. and Brooks, R. 2006. Sexual coercion and the opportunity for sexual selection in guppies. Animal Behaviour, 71: 515–522.CrossRefGoogle Scholar
Heinze, J. and Schrempf, A. 2012. Terminal investment: individual reproduction of ant queens increases with age. Public Library of Science One, 7: e35201.Google ScholarPubMed
Hercus, M.J. and Hoffmann, A.A. 2000. Maternal and grandmaternal age influence offspring fitness in Drosophila. Proceedings of Royal Society London B, 267: 2105–2110.CrossRefGoogle ScholarPubMed
Holland, B. and Rice, W.R. 1999. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proceedings of Natural Academy of Sciences of the United States of America, 96: 5083–5088.CrossRefGoogle ScholarPubMed
Holveck, M.J., Gauthier, A.L.,and Nieberding, C.M. 2015. Dense, small and male biased cages exacerbate male-male competition and reduce female choosiness in Bicyclus anynana. Animal Behaviour, 104: 229–245.CrossRefGoogle Scholar
Johnson, S.L. and Gemmell, N.J. 2012. Are old males still good males and can females tell the difference? Do hidden advantages of mating with old males off-set costs related to fertility. Bioessays, 34: 609–619.CrossRefGoogle ScholarPubMed
Jones, T.M. and Elgar, M.A. 2004. The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle. Proceedings of Royal Society London Biological Sciences, 271: 1311–1318.CrossRefGoogle ScholarPubMed
Jormalainen, V., Tuomi, J., and Yamamura, N. 1994. Intersexual conflict over precopula duration in mate-guarding Crustacea. Behavioural Processes, 32: 265–284.CrossRefGoogle ScholarPubMed
Kern, S., Ackermann, M., Stearns, S.C., and Kawecki, T.J. 2001. Decline in offspring viability as a manifestation of ageing in Drosophila melanogaster. Evolution, 55: 1822–1831.CrossRefGoogle Scholar
Kindlmann, P., Dixon, A.F.G., and Dostálková, I. 2001. Role of ageing and temperature in shaping reaction norms and fecundity functions in insects. Journal of Evolutionary Biology, 14: 835–840.CrossRefGoogle Scholar
Kirkpatrick, M. 1987. Sexual selection by female choice in polygynous animals. Annual Review of Ecology and Systematics, 18, 43–70.CrossRefGoogle Scholar
Kokko, H. and Lindstrom, J. 1996. Evolution of female preference for old mates. Proceedings of Royal Society London, 263: 1533–1538.Google Scholar
Krupa, J.J. and Sih, A. 1993. Experimental studies on water strider mating dynamics: spatial variation in density and sex ratio. Behavioral Ecology and Sociobiology, 33: 107–120.CrossRefGoogle Scholar
Kvarnemo, C., Forsgren, E., and Magnhagen, C. 1995. Effects of sex ratio on intra- and inter-sexual behaviour in sand gobies. Animal Behaviour, 50: 1455–1461.CrossRefGoogle Scholar
Maklakov, A.A., Kremer, N., and Arnqvist, G. 2007. The effects of age at mating on female life-history traits in a seed beetle. Behavioral Ecology, 18: 551–555.CrossRefGoogle Scholar
Manning, J.T. 1985. Choosy females and correlates of male age. Journal of Theoretical Biology, 116: 349–354.CrossRefGoogle Scholar
Mishra, G. and Omkar, 2004. Influence of parental age on reproductive performance of an apidophagous ladybird, Propylea dissecta (Mulsant). Journal of Applied Entomology, 128: 605–609.CrossRefGoogle Scholar
Moore, P.J. and Harris, W.E. 2004. Is a decline in offspring quality a necessary consequence of maternal ageing? Proceedings of Royal Society London Biological Science, 270: 192–194.Google Scholar
Nieberding, C.M., Fischer, K., Saastomoinen, M., Allen, C.E., Wallin, E.A., Adenstrom, E., and Brakefield, P.M. 2012. Cracking the olfactory code of a butterful: the scent of ageing. Ecology Letters, 15: 415–424.CrossRefGoogle ScholarPubMed
Obata, S. 1987. Mating behaviour and sperm transfer in the ladybird beetle. Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Applied Entomology and Zoology, 22: 434–442.CrossRefGoogle Scholar
Omkar, , Pandey, P., Rastogi, S., and Mishra, G. 2010. Influence of age at mating on the reproductive performance of parthenium beetle, Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae). Insect Science, 17: 112–120.CrossRefGoogle Scholar
Omkar, , Pervez, A., Mishra, G., Srivastava, S., Singh, S.K., and Gupta, A.K. 2005. Intrinsic advantages of Cheilomenes sexmaculata over two coexisting Coccinella species (Coleoptera: Coccinellidae). Insect Science, 12: 179–184.CrossRefGoogle Scholar
Pandey, P. and Omkar, . 2013. Age based mate choice improves reproductive performance and offspring attributes in parthenium beetle, Zygogramma bicolorata (Coleoptera: Chrysomelidae). The Canadian Entomologist, 145: 292–301.CrossRefGoogle Scholar
Parker, G.A. 1993. Sperm competition games: sperm size and sperm number under adult control. Proceedings of Royal Society London B, 253: 245–254Google ScholarPubMed
Partridge, L. and Barton, N.H. 1993. Evolution of aging: testing the theory using Drosophila. Genetica, 91: 89–98.CrossRefGoogle ScholarPubMed
Perez-Staples, D., Martinez-Hernandez, M.G., and Aluja, M. 2010. Male age and experience increases mating success but not female fitness in the Mexican fruit fly. Ethology, 116: 778–786.Google Scholar
Pervez, A., Omkar, , and Richmond, A.S. 2004. The influence of age on reproductive performance of a predatory lady bird beetle, Propylea dissecta (Mulsant). Journal of Insect Science, 4: article 22, 1–8.CrossRefGoogle Scholar
Pletcher, S.D. and Curtsinger, J.W. 1998. Mortality plateaus and the evolution of senescence: why are old-age mortality rates so low? Evolution, 52: 454–464.CrossRefGoogle ScholarPubMed
Pound, N. and Gage, M.J. 2004. Prudent sperm allocation in Norway rats, Rattus norvegicus: a mammalian model of adaptive ejaculate adjustment. Animal Behaviour, 68: 819–823.CrossRefGoogle Scholar
Price, D.K. and Hansen, T.F. 1998. How does offspring quality change with age in male Drosophila melanogaster? Behavior Genetics, 28: 395–402.CrossRefGoogle ScholarPubMed
Priest, N.K., Mackowiak, B., and Promislow, D.E.L. 2002. The role of parental age effects on the evolution of ageing. Evolution, 56: 927–935.CrossRefGoogle Scholar
Prohl, H. 2002. Population differences in female resource abundance, adult sex ratio, and male mating success in Dendrobates pumilio. Behavioral Ecology, 13: 175–181.CrossRefGoogle Scholar
Ragland, S.S. and Sohal, R.S. 1973. Mating behaviour, physical activity and ageing in housefly, Musca domestica. Experimental Gerontology, 8: 135–145.CrossRefGoogle ScholarPubMed
Ros, A.F.H., Zeilstra, I., and Oliveira, R.F. 2003. Mate choice in the Galilee St. Peter’s fish, Sarotherodon galilaeus. Behaviour, 140: 1173–1188.Google Scholar
Simmons, L.W. 2001. Sperm competition and its evolutionary consequences in insects. Princeton University Press, Princeton, New Jersey, United States of America.Google Scholar
Simmons, L.W., Emlen, D.J., and Tomkins, J.L. 2007. Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles. Evolution, 61: 2684–2692.CrossRefGoogle ScholarPubMed
Singh, K. and Omkar, 2009. Effect of parental ageing on offspring developmental and survival attributes in an aphidophagous ladybird, Cheilomenes sexmaculata. Journal of Applied Entomology, 133: 500–504.CrossRefGoogle Scholar
Siva-Jothy, M.T. 1987. Variation in copulation duration and the resultant degree of sperm removal in Orthetrum cancellatum (L.) (Libellulidae: Odonata). Behavioral Ecology and Sociobiology, 20: 147–151.CrossRefGoogle Scholar
Siva-Jothy, M.T. and Tsubaki, Y. 1989. Variation in copulation duration in Mnais pruinosa pruinosa Selys (Odonata: Calopterygidae). Behavioral Ecology Sociobiology, 25: 261–267.CrossRefGoogle Scholar
Soares, A.O. and Serpa, A. 2007. Interference competition between ladybird beetle adults (Coleoptera: Coccinellidae): effects on growth and reproductive capacity. Population Ecology, 49: 37–43.CrossRefGoogle Scholar
Srivastava, S. and Omkar, 2004. Age specific mating and reproductive senescence in seven spotted ladybird, Coccinella septempunctata. Journal of Applied Entomology, 128: 452–458.CrossRefGoogle Scholar
Stearns, S.C. 1992. The evolution of life histories. Oxford University Press, London, United Kingdom.Google Scholar
Trivers, R.L. 1972. Parental investment and sexual selection. In Sexual selection and the descent of man 1871–1971. Edited by Campbell, B.. Aldine, Chicago, Illinois, United States of America, Pp. 136–179.Google Scholar
Vargas, G., Michaud, J.P., and Nechols, J.R. 2012. Larval food supply constrains female reproductive schedules in Hippodamia convergens (Coleoptera: Coccinellidae). Annals of the Entomological Society of America, 105: 832–839.CrossRefGoogle Scholar
Weir, L.K., Grant, J.W.A., and Hutchings, J.A. 2011. The influence of operational sex ratio on the intensity of competition for mates. American Naturalist, 177: 167–176.CrossRefGoogle ScholarPubMed
Wenninger, E.J. and Averill, A.L. 2006. Effects of delayed mating on reproductive output of female oriental beetle Anomala orientalis (Coleoptera: Scarabaeidae). Agricultural and Forest Entomology, 8: 221–231.CrossRefGoogle Scholar
Wigby, S., Sirot, L.K., Linklater, J.R., Buehner, N., Calboli, F.C., Bretman, A., and Chapman, T. 2009. Seminal fluid protein allocation and male reproductive success. Current Biology, 19: 751–757.CrossRefGoogle ScholarPubMed
Xu, J. and Wang, Q. 2009. Male moths undertake both pre-and in-copulation mate choice based on female age and weight. Behavioral Ecology and Sociobiology, 63: 801–808.CrossRefGoogle Scholar