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Alternate Reproductive Tactics in an African Dung Beetle, Circellium bacchus (Scarabeidae)

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Abstract

Male-male competition is recognized as a potent force of sexual selection. When intra-sexual competition is strong then selection theory predicts that alternative male phenotypes will evolve. Circellium bacchus is a large, hornless, ball-rolling dung beetle with extensive variation in size and subject to intense male-male contest competition. We proposed that small male C. bacchus, which are unlikely to be successful in male contest competition, would adopt the alternative reproductive tactic of sneaking copulations. This alternative tactic is likely to influence not only behavior, but morphology with an expectation that sneaking males would invest more resources in testes development. Investigation of testis allometry revealed that smaller male C. bacchus beetles had relatively larger testes than their bigger conspecifics. Furthermore, as resources may be limited during larval development, differential investment in testes development should result in adult male beetles either competing for fertilizations or for access to mates. This is seen in C. bacchus as two alternate male phenotypes; smaller beetles with a relatively low body mass invest proportionately more in testes development compared to larger, heavier form in which testes size does not scale with condition. To our knowledge this study provides the first investigation of alternative phenotypes in the reproductive tactics of a ball-rolling dung beetle species.

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References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Birkhead TR (1998) Sperm competition in birds. Rev Reprod 3:123–129

    Article  PubMed  CAS  Google Scholar 

  • Birkhead TR, Atkin L, Møller AP (1987) Copulation behavior of birds. Behavior 101:101–138

    Article  Google Scholar 

  • Byrne PG, Roberts JD, Simmons LW (2002) Sperm competition selects for increased testes mass in Australian frogs. Science 15:347–355

    Google Scholar 

  • Carsten-Conner LD, Papaj DR, O’Brien DM (2010) Resource allocation to testes in walnut flies and implications for reproductive strategy. J Insect Physiol 56:1523–1539

    Article  PubMed  CAS  Google Scholar 

  • Chown SL, Scholtz CH, Klok CJ, Joubert FJ, Coles KS (1995) Ecophysiology, range contraction and survival of a geographically restricted African dung beetle (Coleoptera: Scarabaeidae). Funct Ecol 9:30–39

    Article  Google Scholar 

  • Cook D (1988) Sexual selection in dung beetles. II. Female fecundity as an estimate of male reproductive success in relation to horn size, and alternative behavioural strategies in Onthophagus binodis Thunberg (Scarabaeidae: Onthophagini). Aust J Zool 36:521–523

    Article  Google Scholar 

  • Darwin C (1871) The descent of man and the selection in relation to sex. John Murry, London

    Book  Google Scholar 

  • Deutsch JC (1997) Color diversification in Malawi cichlids: evidence for adaptation, reinforcement or sexual selection? Biol J Linn Soc 62:1–14

    Article  Google Scholar 

  • Diamond JM (1986) Biology of birds of paradise and bowerbirds. Annu Rev Ecol Syst 17:17–37

    Article  Google Scholar 

  • Eberhard WD, Huber BA, Rodriguez RL, Briceño RD, Salas I, Rodriquez V (1998) One size fits all? Relationships between the size and degree of variation in genetalia and other body parts in twenty species of insects and spiders. Evolution 52:415–431

    Article  Google Scholar 

  • Eberhard WD, Huber BA, Rodriguez RL (1999) Don’t forget the biology: a reply to Green. Evolution 53:1624–1627

    Article  Google Scholar 

  • Emlen DJ (1997) Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behav Ecol Sociobiol 41:335–341

    Article  Google Scholar 

  • Emlen DJ (2001) Costs and the diversification of exaggerated animal structures. Science 291:1534–1536

    Article  PubMed  CAS  Google Scholar 

  • Emlen DJ (2008) The evolution of animal weapons. Annu Rev Ecol Evol Syst 39:387–413

    Article  Google Scholar 

  • Emlen DJ, Nijhout HF (2001) Hormonal control of male horn length dimorphism in Onthophagus taurus (Coleoptera: Scarabaeidae): a second critical period of sensitivity to juvenile hormone. J Insect Physiol 47:1045–1054

    Article  PubMed  CAS  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  PubMed  CAS  Google Scholar 

  • Emlen DJ, Marangelo J, Ball B, Cunningham CW (2005) Diversity in the weapons of sexual selection: Horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060–1084

    PubMed  CAS  Google Scholar 

  • Fabricius JC (1781) Species Insectorum, Vol 2. Hamburg, Kilioni

    Google Scholar 

  • Favilla MF, Nolasco J, Florescano IC, Equihua M (2005) Sperm competition and evidence of sperm fertilization patters in the carrion ball-roller beetle Canthon cyanellus cyanellus LeConte (Scarabaeidae: Scarabaeinae). Behav Ecol Sociobiol 59:38–43

    Article  Google Scholar 

  • Flower J, Cohen L, Jarvis P (1998) Practical statistics for field biology. Wiley, West Sussex

    Google Scholar 

  • Gage MJG (1995) Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proc R Soc Lond B Biol Sci 258:247–254

    Article  Google Scholar 

  • Gilliard ET (1969) Birds of paradise and bower birds. Weidenfeld and Nicholson, London

    Google Scholar 

  • Green AJ (1999) Allometry of genetalia in insects: one size does not fit all. Evolution 53:1621–1624

    Article  Google Scholar 

  • Harcourt AH, Purvis A, Liles L (1995) Sperm competition: mating system, not breeding season, affects testes size of primates. Funct Ecol 9:468–476

    Article  Google Scholar 

  • Knell R (2011) Male contest competition and the evolution of weapons. In: Simmons LW, Ridsill-Smith TJ (eds) Ecology and evolution of dung beetles. Blackwell Publishing Ltd, London, pp 47–66

    Chapter  Google Scholar 

  • Knell RJ, Simmons LW (2010) Mating tactics determine patterns of condition dependence in a dimorphic horned beetle. Proc R Soc B 277:2347–2353

    Article  PubMed  Google Scholar 

  • Kruuk LEB, Slate J, Pemberton JM, Brotherstone S, Guinness F, Clutton-Brock T (2002) Antler size in red deer: heritability and selection but no evolution. Evolution 56:1683–1695

    PubMed  CAS  Google Scholar 

  • Kryger U, Cole KS, Tukker R, Scholtz CH (2006) Biology and ecology of Circellium bacchus (Fabricius 1781) (Coleoptera Scarabaeidae), a South African dung beetle of conservation concern. Trop Zool 19:187–207

    Google Scholar 

  • Lawrence WS (1986) Male choice and competition in Tetraopes tetraophthalmus: effects of local sex ration variation. Behav Ecol Sociobiol 18:289–296

    Article  Google Scholar 

  • Le Roux E, Schlotz C, Kinahan H, Bateman PW (2008) Pre and Post-copulatory mate selection mechanisms in an African dung beetle, Circellium bacchus (Coleoptera: Scarabaeidae). J Insect Behav 21:111–122

    Article  Google Scholar 

  • Longair RW (2004) Tusked males, male dimorphism and nesting behavior in a subsocial Afrotropical wasp, Synagris cornuta, and weapons and dimorphism in the Genus (Hymenoptera/: Vespidae/: Eumeninae). J Kans Entomol Soc 77:528–557

    Article  Google Scholar 

  • Moczek A (2011) Evolution and development: onthophagus beetles and the evolutionary developmental genetics of innovation, allometry and plasticity. In: Simmons LW, Ridsill-Smith TJ (eds) Ecology and evolution of dung beetles. Blackwell Publishing Ltd, London, pp 126–151

    Chapter  Google Scholar 

  • Moczek AP, Nijhout HF (2004) Trade-offs during the development of primary and secondary sexual traits in a horn dimorphic beetle. Am Nat 163:184–191

    Article  PubMed  Google Scholar 

  • Møller AP (1991) Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am Nat 137:882–906

    Article  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Parker GA (1990) Sperm competition games: sneaks and extra-pair copulations. Proc R Soc Long B Biol Sci 22:127–133

    Article  Google Scholar 

  • Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Moller AP (eds) Sperm competition and sexual selection. Academic Press, California, pp 3–54

  • Pitcher TE, Dunn PO, Whittingham LA (2005) Sperm competition and the evolution of testes size in birds. J Evol Biol 18:557–567

    Article  PubMed  CAS  Google Scholar 

  • Pomfret JC, Knell RJ (2006) Sexual selection and horn allometry in the dung beetle Euoniticellus intermedius. Anim Behav 71:567–576

    Article  Google Scholar 

  • Rasmussen JL (1994) The influence of horn and body size on the reproductive behavior of the horned rainbow scarab beetle Phanaeus difformis (Coleoptera: scarabaeidae). J Insect Behav 7:67–82

    Article  Google Scholar 

  • Rebelo T (1998) Limestone Fynbos. In: Low AB, Rebelo AG (eds) Vegetation of South Africa, Lesotho and Swaziland. Department of Environmental Affairs and Tourism, Pretoria

  • Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc B 263:1415–1421

    Article  Google Scholar 

  • Sato H, Hiramatsu K (1993) Mating behaviour and sexual selection in the African ball-rolling scarab Khepher platynotus (Bates) (Coleoptera: Scarabaeidae). J Nat Hist 27:657–668

    Article  Google Scholar 

  • Scholtz CH (2009) Pre-copulatory behavior, sexual attraction, mate selection and co- operative breeding. In: Scholtz CH, Davis ALV, Kryger U (eds) Evolutionary biology and conservation of dung beetles. Pensoft Publishers, Sofia, pp 62–68

    Google Scholar 

  • Simmons LW (2011) Sexual selection after mating: the evolutionary consequences of sperm competition and cryptic female choice in Onthophagines. In: Simmons LW, Ridsill-Smith TJ (eds) Ecology and evolution of dung beetles. Blackwell Publishing Ltd, London, pp 66–86

  • Simmons LW, Emlen DJ (2006) Evolutionary trade-off between weapons and testes. Proc Nat Acad Sci USA 103:16346–16351

    Article  PubMed  CAS  Google Scholar 

  • Simmons LW, García-Conzález F (2008) Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles. Evolution 62:2580–2591

    Article  PubMed  Google Scholar 

  • Simmons LW, Kotiaho JS (2002) Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622–1631

    PubMed  Google Scholar 

  • Simmons LW, Kotiaho JS (2007) The effects of reproduction on courtship, fertility and longevity within and between alternative male mating tactics of the horned beetle Onthophagus binodis. Proc Nat Acad Sci USA 104:16604–16608

    Article  PubMed  CAS  Google Scholar 

  • Simmons LW, Ridsill-Smith TJ (eds) (2011) Ecology and evolution of dung beetles. Blackwell Publishing Ltd, London

    Google Scholar 

  • Simmons LW, Emlen DJ, Tomkins JL (2007) Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles. Evolution 61:2684–2692

    Article  PubMed  Google Scholar 

  • Statistica Version 8.0. (2006). Statsoft Inc., Tulsa, USA

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 1871–1971

    Google Scholar 

  • Turner GF (1994) Speciation mechanisms in Lake Malawi cichlids: a critical review. Ergeb Limnol 44:139–160

    Google Scholar 

  • Tynedale-Biscoe M (1978) Physiological age-grading in females of the dung beetle Euoniticellus intermedius (Reiche) (Coleoptera; Scarabaeidae). Bull Ent Res 68:207–217

    Article  Google Scholar 

  • Vahed K, Parker DJ (2011) The evolution of large testes: sperm competition or male mating rate? Ethology 118:107–117

    Article  Google Scholar 

  • van Oppen MJH, Turner GF, Rico C, Robinson RL, Deutsh JC, Genner M, Hewitt GM (1998) Assortative mating among rock dwelling cichlid fishes supports high estimates of species richness from Lake Malawi. Mol Ecol 7:991–1001

    Article  Google Scholar 

  • Watson NL, Simmons LW (2010) Reproductive competition promotes the evolution of female weaponry. Proc R Soc B 277:2035–2040

    Article  PubMed  Google Scholar 

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Acknowledgements

This research formed a part of work undertaken by the Organization for Tropical Studies (OTS) South Africa Program Fall 2011. We would like to thank OTS for this opportunity and are greatly appreciative of the staff and students who assisted in data collection. In particular we would like to thank Melissa Manus, Gabriella Chateau, and Natasha Kohanzadeh for their invaluable help with the dissections and preliminary data analysis. We would also like to thank the two anonymous reviewers who commented on the manuscript and whose advice helped to improve our manuscript.

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Authors and Affiliations

  1. School of Animal, Plant and Environmental Sciences, University of the Witwatersrand, Private Bag 3, Wits, 2050, South Africa

    Chevonne Reynolds & Marcus J. Byrne

  2. Organization for Tropical Studies, South Africa Program, P.O. Box 33, Skukuza, 1350, South Africa

    Chevonne Reynolds

  3. Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, Cape Town, 7701, South Africa

    Chevonne Reynolds

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  1. Chevonne Reynolds
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Correspondence to Chevonne Reynolds.

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Reynolds, C., Byrne, M.J. Alternate Reproductive Tactics in an African Dung Beetle, Circellium bacchus (Scarabeidae). J Insect Behav 26, 440–452 (2013). https://doi.org/10.1007/s10905-012-9365-1

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  • DOI: https://doi.org/10.1007/s10905-012-9365-1

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