Skip to main content
SpringerLink
Log in

Mechanical reproductive isolation via divergent genital morphology between Carabus insulicola and C. esakii with implications in species coexistence

  • Original article
  • Published:
Population Ecology

Abstract

The mechanical isolation hypothesis predicts that physical incompatibility between divergent reproductive morphologies hinders hybridization between populations. However, evidence for this hypothesis remains scarce. We examined this hypothesis using two parapatric carabid beetles, Carabus insulicola and C. esakii, which are of the subgenus Ohomopterus and exhibit a species-specific genital lock-and-key system. Our interspecific crossing experiment revealed that incompatibility of genital morphologies served as a strong postmating-prezygotic isolation barrier. This isolation was asymmetric: a decrease in female fitness was more costly in the cross with greater genitalic incompatibility between a C. esakii female and a C. insulicola male. These two species share a limited sympatric area, but the mechanism responsible for their coexistence is unclear given no evidence of premating isolation via male mate choice. A comparison of the present results with those of previous studies that quantified reproductive isolation between Ohomopterus species suggest that strong mechanical isolation via genitalic incompatibility plays a major role in species isolation, but that it may be less important in species coexistence.

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

Similar content being viewed by others

References

  • Brown WL Jr, Wilson EO (1956) Character displacement. Syst Zool 5:49–64

    Article  Google Scholar 

  • Butlin RK (1989) Reinforcement of premating isolation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinaure Associates, Sunderland, pp 158–179

    Google Scholar 

  • Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381

    Article  Google Scholar 

  • Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Philos Trans R Soc B-Biol Sci 353:287–305

    Article  CAS  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinaure Associates Inc, Sunderland

    Google Scholar 

  • Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Howard DJ (1993) Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 46–69

    Google Scholar 

  • Ishikawa R (1987) On the function of copulatory organs of Ohomopterus (Coleoptera, Carabidae, genus Carabus). Kontyû 55:202–206

    Google Scholar 

  • Ishikawa R (1991) The evolution of Carabus: divergence and isolating mechanisms. Yasaka-shobo, Tokyo (in Japanese)

    Google Scholar 

  • Ishikawa R, Ujiie M (2000) A revision of Carabus (Ohomopterus) insulicola Chaudoir, 1869 (Coleoptera, Carabidae) in Honshu, Japan. Jpn J Syst Entomol 6:253–297

    Google Scholar 

  • Konuma J, Chiba S (2007) Ecological character displacement caused by reproductive interference. J Theor Biol 247:354–364

    Article  PubMed  Google Scholar 

  • Kubota K (1988) Natural hybridization between Carabus (Ohomopterus) maiyasanus and C. (O.) iwawakianus (Coleoptera, Carabidae). Kontyû 56:233–240

    Google Scholar 

  • Kubota K, Sota T (1998) Hybridization and speciation in the carabid beetles of the subgenus Ohomopterus (Coleoptera, Carabidae, genus Carabus). Res Popul Ecol 40:213–222

    Article  Google Scholar 

  • Kuno E (1992) Competitive exclusion through reproductive interference. Res Popul Ecol 34:275–284

    Article  Google Scholar 

  • Mikkola K (2008) The lock-and-key mechanisms of the internal genitalia of the Noctuidae (Lepidoptera): how are they selected for? Eur J Entomol 105:13–25

    Google Scholar 

  • Nagata N, Kubota K, Yahiro K, Sota T (2007) Mechanical barriers to introgressive hybridization revealed by mitochondrial introgression patterns in Ohomopterus ground beetle assemblages. Mol Ecol 16:4822–4836

    Article  PubMed  CAS  Google Scholar 

  • Okuzaki Y, Takami Y, Sota T (2010) Resource partitioning or reproductive isolation: the ecological role of body size differences among closely related species in sympatry. J Anim Ecol 79:383–392

    Article  PubMed  Google Scholar 

  • Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371

    Article  PubMed  Google Scholar 

  • Porter AH, Shapiro AM (1990) Lock-and-key hypothesis: lack of mechanical isolation in a butterfly (Lepidoptera: Pieridae) hybrid zone. Ann Entomol Soc Am 83:107–114

    Google Scholar 

  • Ramsey J, Bradshaw HD Jr, Schemske DW (2003) Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:1520–1534

    PubMed  Google Scholar 

  • Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465

    Article  PubMed  CAS  Google Scholar 

  • Ribeiro JMC, Spielman A (1986) The satyr effect: a model predicting parapatry and species extinction. Am Nat 128:513–528

    Article  Google Scholar 

  • Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102

    Article  Google Scholar 

  • SAS Institute Inc (2009) JMP version 8. SAS Institute Inc, Cary

    Google Scholar 

  • Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Annu Rev Ecol Evol Syst 34:339–364

    Article  Google Scholar 

  • Shapiro AM, Porter AH (1989) The lock-and-key hypothesis: evolutionary and biosystematic interpretation of insect genitalia. Annu Rev Entomol 34:231–245

    Article  Google Scholar 

  • Sota T (2002) Radiation and reticulation: extensive introgressive hybridization in the carabid beetles Ohomopterus inferred from mitochondrial gene genealogy. Popul Ecol 44:145–156

    Article  Google Scholar 

  • Sota T, Kubota K (1998) Genital lock-and-key as a selective agent against hybridization. Evolution 52:1507–1513

    Article  Google Scholar 

  • Sota T, Nagata N (2008) Diversification in a fluctuating island setting: rapid radiation of Ohomopterus ground beetles in the Japanese Islands. Philos Trans R Soc B-Biol Sci 363:3377–3390

    Article  CAS  Google Scholar 

  • Sota T, Tanabe T (2010) Multiple speciation events in an arthropod with divergent evolution in sexual morphology. Proc R Soc B 277:689–696

    Article  PubMed  Google Scholar 

  • Sota T, Kusumoto F, Kubota K (2000a) Consequences of hybridization between Ohomopterus insulicola and O. arrowianus (Coleoptera, Carabidae) in a segmented river basin: parallel formation of hybrid swarms. Biol J Linnean Soc 71:297–313

    Article  Google Scholar 

  • Sota T, Takami Y, Kubota K, Ujiie M, Ishikawa R (2000b) Interspecific body size differentiation in species assemblages of the carabid subgenus Ohomopterus in Japan. Popul Ecol 42:279–291

    Article  Google Scholar 

  • Sota T, Ishikawa R, Ujiie M, Kusumoto F, Vogler AP (2001) Extensive trans-species mitochondrial polymorphisms in the carabid beetles Carabus subgenus Ohomopterus caused by repeated introgressive hybridization. Mol Ecol 10:2833–2847

    PubMed  CAS  Google Scholar 

  • Takami Y (2002) Mating behavior, insemination and sperm transfer in the ground beetle Carabus insulicola. Zool Sci 19:1067–1073

    Article  PubMed  Google Scholar 

  • Takami Y, Suzuki H (2005) Morphological, genetic and behavioural analyses of a hybrid zone between the ground beetles Carabus lewisianus and C. albrechti (Coleoptera, Carabidae): asymmetrical introgression caused by movement of the zone? Biol J Linnean Soc 86:79–94

    Article  Google Scholar 

  • Takami Y, Nagata N, Sasabe M, Sota T (2007) Asymmetry in reproductive isolation and its effect on directional mitochondrial introgression in the parapatric ground beetles Carabus yamato and C. albrechti. Popul Ecol 49:337–346

    Article  Google Scholar 

  • Tanabe T, Sota T (2008) Complex copulatory behavior and the proximate effect of genital and body size differences on mechanical reproductive isolation in the millipede genus Parafontaria. Am Nat 171:692–699

    Article  PubMed  Google Scholar 

  • Ujiie M, Kubota K, Sota T, Ishikawa R (2005) Parallel formation of hybrid swarms of ground beetles in the genus Carabus (Coleoptera: Carabidae) in adjacent river basins. Entomol Sci 8:429–437

    Article  Google Scholar 

  • Ujiie M, Ishikawa R, Kubota K (2010) Geographical variation of Carabus (Ohomopterus) esakii Csiki, 1927 (Coleoptera, Carabidae) in Japan. Biogeography 12:53–64

    Google Scholar 

  • Usami T, Yokoyama J, Kubota K, Kawata M (2006) Genital lock-and-key system and premating isolation by mate preference in carabid beetles (Carabus subgenus Ohomopterus). Biol J Linnean Soc 87:145–154

    Article  Google Scholar 

  • Yoshimura J, Clark CW (1994) Population dynamics of sexual and resource competition. Theor Popul Biol 45:121–131

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to R. Ishikawa, T. Sota, and M. Ujiie for their cooperation in various ways. Two anonymous reviewers gave many insightful comments and suggestions. This study was partly supported by Grants-in-Aid (11306010, 20248015) to K. Kubota from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

  1. Laboratory of Forest Zoology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo, 113-8657, Japan

    Kôhei Kubota, Kôji Miyazaki & Shiho Ebihara

  2. Graduate School of Human Development and Environment, Kobe University, Tsurukabuto 3-11, Nada-ku, Kobe, 657-8501, Japan

    Yasuoki Takami

Authors
  1. Kôhei Kubota
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kôji Miyazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shiho Ebihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yasuoki Takami
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kôhei Kubota.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kubota, K., Miyazaki, K., Ebihara, S. et al. Mechanical reproductive isolation via divergent genital morphology between Carabus insulicola and C. esakii with implications in species coexistence. Popul Ecol 55, 35–42 (2013). https://doi.org/10.1007/s10144-012-0335-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10144-012-0335-4

Keywords

Search

Navigation