Skip to main content
SpringerLink
Log in

Intraspecific variation of reproductive interference capability in Callosobruchus species

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Reproductive interference (RI) is a negative interspecific interaction caused by reproductive activities. Previous studies have implied that male-male competition increases RI capability, consisting of the male harm-inflicting capability of RI by males (RI infliction) and the female susceptibility to heterospecific male harm (RI resistance). Geographical populations show variations in the intensity of male-male competition and sexual conflict due to the influence of biotic/abiotic factors. We made two predictions: (1) RI capability would vary among conspecific populations, and (2) the degree of RI infliction by males would match that of female RI resistance in geographical strains. To test these predictions, we measured the fecundity of once-mated females in two scenarios: housed with heterospecific males and without males. We performed experiments using six strains from each of two bean weevil species, Callosobruchus maculatus and C. chinensis. The results demonstrated intraspecific variation in RI capability within both Callosobruchus species, but the RI infliction of males and RI resistance of females within a geographical strain did not consistently coincide. Our results suggest that RI varies depending on geographical strains, even within species, but we did not obtain evidence that sexual conflict molds RI capability, indicating traits driving RI do not follow the sexual conflict in both Callosobruchus species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arnqvist G (1992) Spatial variation in selective regimes: sexual selection in the water strider, Gerris odontogaster. Evolution 46:914–929

    Article  PubMed  Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press

    Book  Google Scholar 

  • Arnqvist G, Nilsson T, Katvala M (2005) Mating rate and fitness in female bean weevils. Behav Ecol 16:123–127

    Article  Google Scholar 

  • Bateman A (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  PubMed  Google Scholar 

  • Boiteau G (1985) Bionomics and genetics of a black mutant colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 78:663–666

    Article  Google Scholar 

  • Chapman T, Liddle L, Kalb J et al (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241–244

    Article  CAS  PubMed  Google Scholar 

  • Chapman T, Miyatake T, Smith H, Partridge L (1998) Interactions of mating, egg production and death rates in females of the mediterranean fruitfly, Ceratitis capitata. Proc R Soc Lond B 265:1879–1894

    Article  CAS  Google Scholar 

  • Dougherty L, van Lieshout E, McNamara K et al (2017) Sexual conflict and correlated evolution between male persistence and female resistance traits in the seed beetle Callosobruchus maculatus. Proc Royal Soc B: Biol Sci 284:20170132

    Article  Google Scholar 

  • Eady P (1995) Why do male Callosobruchus maculatus beetles inseminate so many sperm? Behav Ecol Sociobiol 36:25–32

    Article  Google Scholar 

  • Eady P (2000) Copulating with multiple mates enhances female fecundity but not egg-to-adult survival in the Bruchid beetle Callosobruchus maculatus. Evolution 54:2161–2165

    CAS  PubMed  Google Scholar 

  • Endler J (1977) Geographic variation, speciation and clines. (MPB-10), volume 10. Princeton University Press http://www.jstor.org/stable/j.ctvx5wbdg

  • Fox C (1993) Multiple mating, lifetime fecundity and female mortality of the bruchid beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Funct Ecol 203–208

  • Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282

    Article  PubMed  Google Scholar 

  • Harano T, Yasui Y, Miyatake T (2006) Direct effects of polyandry on female fitness in Callosobruchus chinensis. Anim Behav 71:539–548

    Article  Google Scholar 

  • Hotzy C, Arnqvist G (2009) Sperm competition favors harmful males in seed beetles. Curr Biol 19:404–407

    Article  CAS  PubMed  Google Scholar 

  • Hotzy C, Polak M, Rönn J, Arnqvist G (2012) Phenotypic engineering unveils the function of genital morphology. Curr Biol 22:2258–2261

    Article  CAS  PubMed  Google Scholar 

  • Kashiwagi M, Utida S (1972) A new mutant in Callosobruchus chinensis L. (Coleoptera: Bruchidae). Appl Entomol Zool 7:95–96

    Article  Google Scholar 

  • Kishi S, Nishida T, Tsubaki Y (2009) Reproductive interference determines persistence and exclusion in species interactions. J Anim Ecol 78:1043–1049

    Article  PubMed  Google Scholar 

  • Kondo N, Tuda M, Toquenaga Y et al (2011) Wolbachia infections in world populations of bean beetles (Coleoptera: Chrysomelidae: Bruchinae) infesting cultivated and wild legumes. Zoolog Sci 28:501–509

    Article  PubMed  Google Scholar 

  • Kyogoku D (2021) Seed beetles as a modern model system of interspecific competition. Ecol Res 36:580–589

    Article  Google Scholar 

  • Kyogoku D, Nishida T (2013) The mechanism of the fecundity reduction in Callosobruchus maculatus caused by Callosobruchus chinensis males. Popul Ecol 55:87–93

    Article  Google Scholar 

  • Kyogoku D, Sota T (2015) Does heterospecific seminal fluid reduce fecundity in interspecific copulation between seed beetles? J Insect Physiol 72:54–60

    Article  CAS  PubMed  Google Scholar 

  • Kyogoku D, Sota T (2015) Exaggerated male genitalia intensify interspecific reproductive interference by damaging heterospecific female genitalia. J Evol Biol 28:1283–1289

    Article  CAS  PubMed  Google Scholar 

  • Kyogoku D, Sota T (2017) The evolution of between-species reproductive interference capability under different within-species mating regimes. Evolution 71:2721–2727

    Article  PubMed  Google Scholar 

  • Mano H, Toquenaga Y (2008) Wall-making behavior as a proximate mechanism to generate variation in larval competition in Callosobruchus maculatus (Coleoptera: Bruchidae). Evol Ecol 22:177–191

    Article  Google Scholar 

  • Messina F, Mitchell R (1989) Intraspecific variation in the egg-spacing behavior of the seed beetleCallosobruchus maculatus. Journal of Insect Behavior 2:727–742

    Article  Google Scholar 

  • Miyatake T, Matsumura F (2004) Intra-specific variation in female remating in Callosobruchus chinensis and C. maculatus. J Insect Physiol 50:403–408

    Article  CAS  PubMed  Google Scholar 

  • Nishida S, Hashimoto K, Kanaoka M et al (2017) Variation in the strength of reproductive interference from an alien congener to a native species in Taraxacum. J Plant Res 130:125–134

    Article  PubMed  Google Scholar 

  • Numajiri Y, Kondo N, Toquenaga Y (2017) Melanic mutation causes a fitness decline in bean beetles infected by Wolbachia. Entomol Exp Appl 164:54–65

    Article  CAS  Google Scholar 

  • Pascoal S, Mendrok M, Wilson A et al (2017) Sexual selection and population divergence II. Divergence in different sexual traits and signal modalities in field crickets (Teleogryllus oceanicus). Evolution 71:1614–1626

    Article  PubMed  Google Scholar 

  • Price T, Leonard A, Lancaster L (2017) Warp-speed adaptation to novel hosts after 300 generations of enforced dietary specialisation in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Eur J Entomol

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/

  • Rönn J, Katvala M, Arnqvist G (2007) Coevolution between harmful male genitalia and female resistance in seed beetles. Proc Natl Acad Sci 104:10921–10925

    Article  PubMed  PubMed Central  Google Scholar 

  • Shimomura K, Mimura T, Ishikawa S et al (2010) Variation in mate recognition specificities among four Callosobruchus seed beetles. Entomol Exp Appl 135:315–322

    Article  Google Scholar 

  • Takano M, Toquenaga Y, Fujii K (2001) Polymorphism of competition type and its genetics in Callosobruchus maculatus (Coleoptera: Bruchidae). Popul Ecol 43:265–273

    Article  Google Scholar 

  • Terry M (2022)A package for survival analysis in https://CRAN.R-project.org/package=survival

  • Terry M, Patricia M (2000) Modeling survival data: extending the Cox model. Springer, New York

    Google Scholar 

  • Thanthianga C, Mitchell R (1990) The fecundity and oviposition behavior of a south indian strain of Callosobruchus maculatus. Entomol Exp Appl 57:133–142

    Article  Google Scholar 

  • Toquenaga Y (1993) Contest and scramble competitions in Callosobruchus maculatus (Coleoptera: Bruchidae) II. Larval competition and interference mechanisms. Popul Ecol 35:57–68

    Article  Google Scholar 

  • Toquenaga Y, Fujii K (1991) Contest and scramble competitions in callosobruchus maculatus (Coleoptera: Bruchidae). Popul Ecol 33:199–211

    Article  Google Scholar 

  • Ursprung C, Den Hollander M, Gwynne D (2009) Female seed beetles, Callosobruchus maculatus, remate for male-supplied water rather than ejaculate nutrition. Behav Ecol Sociobiol 63:781–788

    Article  Google Scholar 

  • Utida S (1941) Studies on experimental population of the azuki bean weevil, Callosobruchus chinensis (L.) I. The effect of population density on the progeny populations. Mem College Agric, Kyoto Imp Univ 48:1–30

    Google Scholar 

  • Van Haren M, Rönn J, Schilthuizen M, Arnqvist G (2017) Postmating sexual selection and the enigmatic jawed genitalia of Callosobruchus subinnotatus. Biology Open 6:1008–1012

    PubMed  PubMed Central  Google Scholar 

  • Yassin A, David J (2016) Within-species reproductive costs affect the asymmetry of satyrization in Drosophila. J Evol Biol 29:455–460

    Article  CAS  PubMed  Google Scholar 

  • Yun L, Agrawal A, Rundle H (2021) On male harm: How it is measured and how it evolves in different environments

Download references

Funding

This study was supported, in part, by Grants-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (Nos. 14405003, 17405005, 17570014, 20405006, 23405008, 23570017, 26304016, and 17H04612 to Y.T.).

Author information

Authors and Affiliations

  1. Doctoral Program in Biology, University of Tsukuba, Tsukuba, Ibaraki, Japan

    Wataru Mukaimine

  2. Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan

    Yukihiko Toquenaga

Authors
  1. Wataru Mukaimine
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yukihiko Toquenaga
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wataru Mukaimine.

Ethics declarations

Conflicts of interest

We declare we have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

We are grateful to Koichi Fujii, Masakazu Shimada, and Frank Messina for dispensing the strains of bean weevils which we used. We would like to thank Editage (www.editage.com) for English language editing.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (docx 127 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mukaimine, W., Toquenaga, Y. Intraspecific variation of reproductive interference capability in Callosobruchus species. Evol Ecol 37, 531–544 (2023). https://doi.org/10.1007/s10682-022-10223-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-022-10223-3

Keywords

Search

Navigation