Does seed size mediate sex-specific reproduction costs in the Callosobruchus maculatus bean beetle?

Autoři: Dariusz Krzysztof Małek aff001;  Maciej Jan Dańko aff002;  Marcin Czarnoleski aff001
Působiště autorů: Institute of Environmental Sciences, Jagiellonian University, Kraków, Poland aff001;  Max Planck Institute for Demographic Research, Rostock, Germany aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


There is a trade-off between reproductive effort and adult longevity, and when resource allocation is taken into account, it is especially pronounced in species that have aphagous adult forms. This trade-off may be further complicated by environmental factors such as nutrient availability during larval development and by the other sex, which influences the costs of reproduction due to the presentation of nuptial gifts. Here, we examined the influence of larval nutrient quantity on the sex-specific longevity costs of reproduction in the gift-giving seed beetle Callosobruchus maculatus. We found no indication that differences in the nutrient quality of larger and smaller host seeds influence survival in virgin and reproducing individuals or nuptial gift size in reproducing individuals. However, in the case of reproducing individuals, the effect of seed size on survival was statistically marginal. Therefore, we advise taking this into account when investigating reproductive efforts in this species. We have also observed interesting interactions between male and female reproductive costs. While females had generally higher mortality than males, nuptial gifts resulted in lowered female mortality and increased male mortality. Additionally, we found a possibly non-linear relationship between nuptial gift size and the offspring production rate of female recipients.

Klíčová slova:

Beetles – Copulation – Death rates – Larvae – Reproductive physiology – Sperm – Beans – Reproductive success


1. Reznick D. Costs of Reproduction: An Evaluation of the Empirical Evidence. Oikos. 1985;44(2):257–67. Available from:

2. Roff DA. The evolution of life histories: theory and analysis. Vol. 3, Reviews in Fish Biology and Fisheries. 1992. 535 p.

3. Stearns SC. The evolution of life histories. Vol. 1, Oxford University Press. 1992. 249 p.

4. Perrin N, Sibly RM. Dynamic-Models of Energy Allocation and Investment. Annu Rev Ecol Syst. 1993;24:379–410.

5. Cichoń M. Evolution of longevity through optimal resource allocation. Proc R Soc London B Biol Sci. 1997;264(1386):1383–8.

6. Dańko MJ, Burger O, Kozłowski J. Density-dependence interacts with extrinsic mortality in shaping life histories. PLoS One. 2017;12(10).

7. Charnov EL. The theory of sex allocation. Monogr Popul Biol. 1982;18:1–355. 7144766

8. Scharf I, Peter F, Martin OY. Reproductive Trade-Offs and Direct Costs for Males in Arthropods. Evol Biol. 2013;40(2):169–84.

9. Sprung M. Costs of reproduction: A study on metabolic requirements of the gonads and fecundity of the bivalve Dreissena polymorpha. Malacologia. 1991;33(1–2):63–70.

10. Lewis SM, Vahed K, Koene JM, Engqvist L, Bussière LF, Perry JC, et al. Emerging issues in the evolution of animal nuptial gifts. Biol Lett. 2014;10(7):20140336–. doi: 10.1098/rsbl.2014.0336 25030043

11. Gwynne DT. Sexual conflict over nuptial gifts in insects. Annu Rev Entomol. 2008;53:83–101. doi: 10.1146/annurev.ento.53.103106.093423 17680720

12. Voigt CC, Michener R, Kunz TH. The energetics of trading nuptial gifts for copulations in katydids. Physiological and Biochemical Zoology, 2005; 78(3), 417–423. doi: 10.1086/430224 15887088

13. Tatar M, Carey JR. Nutrition mediates reproductive trade-offs with age-specific mortality in the beetle Callosobruchus maculatus. Ecology. 1995;76(7):2066–73.

14. Calow P. The Relationship between Fecundity, Phenology, and Longevity: A Systems Approach. Am Nat. 1973;107(956):559–74.

15. Immonen E, Hoikkala A, Kazem AJ, Ritchie MG. 2009. When are vomiting males attractive? Sexual selection on condition-dependent nuptial feeding in Drosophila subobscura. Behavioral Ecology, 2009; 20(2), 289–295.

16. Engqvist L. Sex, food and conflicts: nutrition dependent nuptial feeding and pre-mating struggles in scorpionflies. Behavioral Ecology and Sociobiology, 2007; 61(5), 703–710.

17. Field SA, Yuval B. Nutritional status affects copula duration in the Mediterranean fruit fly, Ceratitis capitata (Insecta Tephritidae). Ethology Ecology & Evolution 1999;11.1: 61–70.

18. Messina FJ. Life-history variation in a seed beetle: adult egg-laying vs. larval competitive ability. Oecologia. 1991;85(3):447–55. doi: 10.1007/BF00320624 28312053

19. Eady PE. Why do male Callosobruchus maculatus beetles inseminate so many sperm? Behav Ecol Sociobiol. 1995;36(1):25–32.

20. Savalli UM, Fox CW. The effect of male mating history on paternal investment, fecundity and female remating in the seed beetle Callosobruchus maculatus. Funct Ecol. 1999;13(2):169–77.

21. Fox CW, Stillwell RC, Wallin WG, Hitchcock LJ. Temperature and host species affect nuptial gift size in a seed-feeding beetle. Funct Ecol. 2006;20(6):1003–11.

22. Martinossi‐Allibert I, Arnqvist G, Berger D. "Sex‐specific selection under environmental stress in seed beetles." Journal of evolutionary biology 2017;30.1: 161–173.

23. Kergoat GJ, Delobel A, Silvain JF. Phylogeny and host-specificity of European seed beetles (Coleoptera, Bruchidae), new insights from molecular and ecological data. Mol Phylogenet Evol. 2004;32(3):855–65. doi: 10.1016/j.ympev.2004.02.019 15288061

24. Giga DP, Smith RH. Intraspecific competition in the bean weevils Callosobruchus maculatus and Callosobruchus rhodesianus (Coleoptera: Bruchidae). Journal of applied ecology, 1991, 918–929.

25. Toquenaga Y. Contest and scramble competitions in Callosobruchus maculatus (Coleoptera: Bruchidae) II. Larval competition and interference mechanisms. Population Ecology, 1993, 35.1: 57–68.

26. Fox CW, Bush ML, Wallin WG. Maternal age affects offspring lifespan of the seed beetle, Callosobruchus maculatus. Funct Ecol. 2003;17(6):811–20.

27. Fox CW, Hickman DL, Raleigh EL, Mousseau TA. Paternal investment in a seed beetle (Coleoptera: Bruchidae): Influence of male size, age and mating history. Vol. 88, Entomological Society of America. 1995. p. 100–3.

28. Eady PE, Brown DV. Spermatophore size and mate fecundity in the bruchid beetle Callosobruchus maculatus. Ethol Ecol Evol. 2000;12(2):203–7.

29. Savalli UM, Fox CW. Genetic variation in paternal investment in a seed beetle. Anim Behav. 1998;56(4):953–61. doi: 10.1006/anbe.1998.0853 9790706

30. R Core Team. 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.2019. Available from:

31. Ferrari SLP, Cribari-Neto F. Beta regression for modelling rates and proportions. J Appl Stat. 2004;31(7):799–815.

32. Vaupel JW, Manton KG, Stallard E. The impact of heterogeneity in individual frailty on the dynamics of mortality. Vol. 16, Demography. 1979. p. 439–54. 510638

33. Duchateau L, Janssen P, Gail M, Krickeberg K, Sarmet J, Tsiatis A, et al. The frailty model. The Frailty Model. 2008. 1–316 p.

34. Aalen OO, Borgan O, Gjessing HK. Survival and Event History Analysis: A Process Point of View. Book. 2008. 540 p.

35. Hougaard P. Analysis of Multivariate Survival Data. Biometrika [Internet]. 2000;68(2):542.

36. Grambsch PM, Therneau TM. Proportional hazards tests and diagnostics based on weighted residuals. Biometrika. 1994;81(3):515–26.

37. Andersen PK, Gill RD. Cox’s Regression Model for Counting Processes: A Large Sample Study. Ann Stat. 1982;10(4):1100–20.

38. Therneau TM, Grambsch PM. Modeling Survival Data: Extending the Cox Model. Springer-Verlag; 2000.

39. Munda M, Rotolo F, Legrand C. parfm: Parametric Frailty Models in R. J Stat Softw. 2012;51(11):1–20.

40. Burnham KP editor Anderson DR. Model Selection and Multimodel Inference A Practical Information-Theoretic Approach. MODEL SELECTION & MULTIMODEL INFERENCE. 2002.

41. Therneau TM, Grambsch PM, Fleming TR. Martingale-based residuals for survival models. Biometrika. 1990;77(1):147–60.

42. Davis C, Hyde J, Bangdiwala S, Nelson J. An example of dependencies among variables in a conditional logistic regression. In: Moolgavkar S, editor. Modern Statistical Methods in Chronic Disease Epidemiology. New York: Wiley; 1986.

43. Harrell FE. Regression Modeling Strategies. Vol. 64, Springer Series in Statistics. 2015. 501–507 p.

44. Wood SN. Generalized additive models: an introduction with R. Texts Stat Sci. 2006;xvii, 392 p.

45. Knowles JE, Frederick C. (2016). merTools: tools for analyzing mixed effect regression models. R package version 0.3. 0.

46. Cope JM, Fox CW. Oviposition decisions in the seed beetle, Callosobruchus maculatus (Coleoptera: Bruchidae): Effects of seed size on superparasitism. J Stored Prod Res. 2003;39(4):355–65.

47. Credland PF, Dick KM, Wright AW. Relationships between larval density, adult size and egg production in the cowpea seed beetle, Callosobruchus maculatus. Ecol Entomol. 1986;11(1):41–50.

48. Rönn JL, Katvala M, Arnqvist G. Interspecific variation in ejaculate allocation and associated effects on female fitness in seed beetles. Journal of evolutionary biology, 2008, 21.2: 461–470.

49. Katvala M, Rönn JL, Arnqvist G. Correlated evolution between male ejaculate allocation and female remating behaviour in seed beetles (Bruchidae). Journal of evolutionary biology, 2008, 21.2: 471–479.

50. Paukku S, Kotiaho JS. Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity. Journal of Insect Physiology, 2005, 51.11: 1220–1226.

51. Fox CW, Dublin L, Pollitt SJ. Gender differences in lifespan and mortality rates in two seed beetle species. Funct Ecol. 2003;17(5):619–26.

52. Berg EC. Maklakov AA. Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle. Proceedings of the Royal Society B: Biological Sciences, 2012, 279.1745: 4296–4302.

53. Rönn J. Katvala M. Arnqvist G. The costs of mating and egg production in Callosobruchus seed beetles. Animal Behaviour, 2006, 72.2: 335–342.

54. Eady PE, Hamilton L. Lyons RE. Copulation, genital damage and early death in Callosobruchus maculatus. Proceedings of the Royal Society B: Biological Sciences, 2006, 274.1607: 247–252.

55. Hotzy C, Arnqvist G. Sperm competition favors harmful males in seed beetles. Current Biology, 2009, 19.5: 404–407.

56. Ursprung C, Den Hollander M, Gwynne DT. Female seed beetles, Callosobruchus maculatus, remate for male-supplied water rather than ejaculate nutrition. Behav Ecol Sociobiol. 2009;63(6):781–8.

57. Fox CW. Multiple Mating, Lifetime Fecundity and Female Mortality of the Bruchid Beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Funct Ecol. 1993;7(2):203.

58. Fritzsche K, Arnqvist G. Homage to Bateman: sex roles predict sex differences in sexual selection. Evolution, 2013, 67.7: 1926–1936.

59. Katsuki M; Toquenaga Y, Miyatake T. Larval competition causes the difference in male ejaculate expenditure in Callosobruchus maculatus. Population ecology, 2013, 55.3: 493–498.

60. Savalli UM, Czesak ME, Fox CW. Paternal investment in the seed beetle Callosobruchus maculatus (Coleoptera: Bruchidae): variation among populations. Annals of the Entomological Society of America, 2000, 93.5: 1173–1178.

61. Hall MD, BussiÈre LF, Brooks R. Diet-dependent female evolution influences male lifespan in a nuptial feeding insect. J Evol Biol. 2009;

62. Moya-Laraño J, Fox CW. Ejaculate size, second male size, and moderate polyandry increase female fecundity in a seed beetle. Behav Ecol. 2006;17(6):940–6.

63. Honěk A. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos, 1993, 483–492.

64. Fox CW. Multiple Mating, Lifetime Fecundity and Female Mortality of the Bruchid Beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Funct Ecol. 1993;7(2):203.

65. Rönn JL, Katvala M, Arnqvist G. Correlated evolution between male and female primary reproductive characters in seed beetles. Functional Ecology, 2011, 25.3: 634–640.

66. Wilson N, Tubman SC, Eady PE, Robertson GW Female genotype affects male success in sperm competition. Proceedings of the Royal Society of London. Series B: Biological Sciences, 1997, 264.1387: 1491–1495.

67. Birkhead TR. Cryptic female choice: criteria for establishing female sperm choice. Evolution, 1998, 52.4: 1212–1218.

68. Rönn J, Katvala M, Arnqvist G. Coevolution between harmful male genitalia and female resistance in seed beetles. Proceedings of the National Academy of Sciences, 2007, 104.26: 10921–10925.

69. Edvardsson M, Canal D. The effects of copulation duration in the bruchid beetle Callosobruchus maculatus. Behavioral Ecology, 2006, 17.3: 430–434.

70. Miyatake T, Matsumura F. Intra-specific variation in female remating in Callosobruchus chinensis and C. maculatus. Journal of Insect Physiology, 2004, 50.5: 403–408.

71. Savalli UM, Fox CW. The effect of male size, age, and mating behavior on sexual selection in the seed beetle Callosobruchus maculatus. Ethology Ecology & Evolution, 1999, 11.1: 49–60.

72. Fox CW, Moya‐Laraño J. Diet affects female mating behaviour in a seed‐feeding beetle. Physiological Entomology, 2009, 34.4: 370–378.

73. Ursprung C, Den Hollander M, Gwynne DT. Female seed beetles, Callosobruchus maculatus, remate for male-supplied water rather than ejaculate nutrition. Behav Ecol Sociobiol. 2009;63(6):781–8.

74. Edvardsson M. Female Callosobruchus maculatus mate when they are thirsty: resource-rich ejaculates as mating effort in a beetle. Animal Behaviour, 2007, 74.2: 183–188.

75. Bayram H, Sayadi A, Goenaga J, Immonen E, Arnqvist G. Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach. Insect molecular biology, 2017, 26.1: 58–73.

76. Bayram H, Sayadi A, Immonen E, Arnqvist G. Identification of novel ejaculate proteins in a seed beetle and division of labour across male accessory reproductive glands. Insect biochemistry and molecular biology, 2019, 104: 50–57. doi: 10.1016/j.ibmb.2018.12.002 30529580

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