Sexual Selection, Ontogenetic Acceleration, and Hypermorphosis Generates Male Trimorphism in Wellington Tree Weta

Abstract

Strong sex-specific selection on traits common to both sexes typically results in sexual dimorphism. Here we find that Wellington tree weta (Hemideina crassidens) are sexually dimorphic in both head shape and size due to differential selection pressures on the sexes: males use their heads in male-male combat and feeding whereas females use theirs for feeding only. Remarkably, the sexes share a common ontogenetic trajectory with respect to head growth. Male head shape allometry is an extension of the female’s trajectory despite maturing two instars earlier, a feat achieved through ontogenetic acceleration and hypermorphosis. Strong sexual selection also favours the evolution of alternative reproductive strategies in which some males produce morphologically different weapons. Wild-caught male H. crassidens are trimorphic with regard to weapon size, a rare phenomenon in nature, and weapon shape is related to each morph’s putative mating strategy.

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References

  1. Adams, D. C. (2010). Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evolutionary Biology, 10(72), 1–10.

    Google Scholar 

  2. Adams, D. C., & Collyer, M. (2009). A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution, 63, 1143–1154.

    Article  PubMed  Google Scholar 

  3. Adams, D. C., & Nistri, A. (2010). Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology, 10(216), 1–10.

    Google Scholar 

  4. Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71, 5–16.

    Article  Google Scholar 

  5. Alberch, P., Gould, S., Oster, G., & Wake, D. (1979). Size and shape in ontogeny and phylogeny. Paleobiology, 5, 296–317.

    Google Scholar 

  6. Allen, B., & Levinton, J. (2007). Costs of bearing a sexually selected ornamental weapon in a fiddler crab. Functional Ecology, 21, 154–161.

    Article  Google Scholar 

  7. Anderson, M. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.

    Article  Google Scholar 

  8. Andersson, M. (1994). Sexual selection. Princeton, New Jersey: Princeton University Press.

    Google Scholar 

  9. Benaglia, T., Chauveau, D., Hunter, D. R., & Young, D. S. (2009). mixtools: An R package for analyzing finite mixture models. Journal of Statistical Software, 32, 1–29.

    Google Scholar 

  10. Berner, D., Adams, D. C., Grandchamp, A., & Hendry, A. (2008). Natural selection drives patterns of lake-stream divergence in stickleback foraging morphology. Journal of Evolutionary Biology, 21, 1653–1665.

    CAS  Article  PubMed  Google Scholar 

  11. Blanckenhorn, W. U. (2005). Behavioral causes and consequences of sexual size dimorphism. Ethology, 111, 977–1016.

    Article  Google Scholar 

  12. Bookstein, F. L. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  13. Bookstein, F., Schafer, K., Prossinger, H., Seidler, H., Fieder, M., Stringer, C., et al. (1999). Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. Anatomical Record, 257, 217–224.

    Google Scholar 

  14. Claude, J. (2008). Morphometrics with R. New York, NY: Springer.

    Google Scholar 

  15. Claverie, T., & Smith, I. (2010). Allometry and sexual dimorphism in the chela shape in the squat lobster munida rugosa. Aquatic Biology, 8, 179–187.

    Article  Google Scholar 

  16. Correa, C., Baeza, J., Dupre, E., Hinojosa, I., & Thiel, M. (2000). Mating behavior and fertilization success of three ontogenetic stages of male rock shrimp Rhynchocinetes typus (Decapoda: Caridea). Journal of Crustacean Biology, 20, 628–640.

    Article  Google Scholar 

  17. Emlen, D. J. (2008). The evolution of animal weapons. Annual Reviews in Ecology, Evolution and Systematics, 39, 387–413.

    Article  Google Scholar 

  18. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223.

    CAS  Article  PubMed  Google Scholar 

  19. Fairbairn, D. J. (1990). Factors influencing sexual size dimorphism in temperate waterstriders. American Naturalist, 136, 61–86.

    Article  Google Scholar 

  20. Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: Pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics, 28, 659–687.

    Article  Google Scholar 

  21. Fairbairn, D. J., & Preziosi, R. F. (1994). Sexual selection and the evolution of allometry for sexual size dimorphism in the water strider, Aquarius remigis. American Naturalist, 144, 101–118.

    Article  Google Scholar 

  22. Field, L. H., & Deans, N. A. (2001). Sexual selection and secondary sexual characters of wetas and king crickets. In L. H. Field (Ed.), The Biology of Wetas, King Crickets and their Allies (pp. 179–204). Wallingford: CAB International.

    Chapter  Google Scholar 

  23. Field, L. H., & Sandlant, G. R. (2001). The gallery-related ecology of New Zealand tree wetas, Hemideinafemorata and Hemideinacrassidens (Orthoptera, Anostostomatidae). In L. H. Field (Ed.), The biology of Wetas, King Crickets and their allies (pp. 243–257). Wallingford: CAB International.

    Chapter  Google Scholar 

  24. Gibbs, G. W. (2001). Habitats and biogeography of New Zealand’s Deinacridine and tusked weta species. In L. H. Field (Ed.), The biology of Wetas, King Crickets and their allies (pp. 35–55). Wallingford: CAB International.

    Chapter  Google Scholar 

  25. Gwynne, D. T., & Jamieson, I. (1998). Sexual selection and sexual dimorphism in a harem-polygynous insect, the alpine weta (Hemideina maori, Orthoptera Stenopelmatidae). Ethology, Ecology & Evolution, 10, 393–402.

    Article  Google Scholar 

  26. Hens, S. (2005). Ontogeny of craniofacial sexual dimorphism in the orangutan (pongo pygmaeus). I: Face and palate. American Journal of Primataology, 65, 149–166.

    Article  Google Scholar 

  27. Herler, J., Kerschbaumer, M., Mitteroecker, P., Postl, L., & Sturmbauer, C. (2010). Sexual dimorphism and population divergence in the lake tanganyika cichlid fish genus tropheus. Frontiers in Zoology, 7, 4.

    Article  PubMed  Google Scholar 

  28. Huyghe, K., Herrel, A., Vanhooydonck, B., & Van, D. R. (2007). It’s all in the head: Morphological basis for differences in bite force among color morphs of the dalmatian wall lizard. Journal of Morphology, 268, 1088–1089.

    Google Scholar 

  29. Kaliontzopoulou, A., Carretero, M., & Liorentel, G. (2007). Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in podarcis lizards. Journal of Morphology, 268, 152–165.

    Article  PubMed  Google Scholar 

  30. Kallman, K. D. (1984). A new look at sex determination in poeciliid fishes. In B. J. Turner (Ed.), Evolutionary genetics of fishes (pp. 95–171). New York, NY: Plenum Publishing Co. Inc.

    Google Scholar 

  31. Kelly, C. D. (2005a). Allometry and sexual selection of male weaponry in Wellington tree weta, Hemideina crassidens. Behavioral Ecology, 16, 145–152.

    Article  Google Scholar 

  32. Kelly, C. D. (2005b). Sexual selection and infection by ectoparasites in Wellington tree weta, Hemideina crassidens (Orthoptera: Anostostomatidae). Austral Ecology, 30, 648–654.

    Article  Google Scholar 

  33. Kelly, C. D. (2006a). Fighting for harems: Assessment strategies during male-male contests in the sexually dimorphic Wellington tree weta. Animal Behaviour, 72, 727–736.

    Article  Google Scholar 

  34. Kelly, C. D. (2006b). The relationship between resource control, association with females and male weapon size in a male dominance insect. Ethology, 112, 362–369.

    Article  Google Scholar 

  35. Kelly, C. D. (2008a). Identifying a causal agent of sexual selection on weaponry in an insect. Behavioral Ecology, 19, 184–192.

    Article  Google Scholar 

  36. Kelly, C. D. (2008b). The interrelationships between resource-holding potential, resource-value and reproductive success in territorial males: How much variation can we explain? Behavioral Ecology and Sociobiology, 62, 855–871.

    Google Scholar 

  37. Lande, R. (1980). Sexual dimorphism, sexual selection, and adaption in polygenic characters. Evolution, 34, 292–305.

    Article  Google Scholar 

  38. Lappin, A., Hamilton, P., & Sullivan, B. (2006). Bite-force performance and head shape in a sexually dimorphic crevice-dwelling lizard, the common chuckwalla [Sauromalus ater (=obesus)]. Biological Journal of the Linnean Society, 88, 215–222.

    Article  Google Scholar 

  39. McLachlan, G. J., & Basford, K. E. (1988). Mixture models: Inference and applications to clustering. New York, NY: Marcel Dekker, Inc.

    Google Scholar 

  40. Mitteroecker, P., & Bookstein, F. (2008). The evolutionary role of modularity and integration in the hominoid cranium. Evolution, 62, 943–958.

    Article  PubMed  Google Scholar 

  41. Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., & Bookstein, F. (2004). Comparison of cranial ontogenetic trajectories among great apes and humans. Journal of Human Evolution, 46, 679–697.

    Article  PubMed  Google Scholar 

  42. Navarro, J., Kaliontzopoulou, A., & Gonzalez-Solis, J. (2009). Sexual dimorphism in bill morphology and feeding ecology in cory’s shearwater (Calonectris diomedea). Zoology, 112, 128–138.

    Article  PubMed  Google Scholar 

  43. Oliveira, R. F., Taborsky, M., & Brockmann, H. J. (Eds.). (2008). Alternative reproductive tactics: An integrative approach. Cambridge: Cambridge University Press.

    Google Scholar 

  44. Oufiero, C., & Garland, T. (2007). Evaluating performance costs of sexually selected traits. Functional Ecology, 21, 676–689.

    Article  Google Scholar 

  45. R Development Core Team. (2009). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  46. Rohlf, F., & Marcus, L. (1993). A revolution in morphometrics. Trends in Ecology & Evolution, 8, 129–132.

    Article  Google Scholar 

  47. Rohlf, F., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.

    Article  Google Scholar 

  48. Rowland, J., & Emlen, D. (2009). Two thresholds, three male forms result in facultative male trimorphism in beetles. Science, 323, 773–776.

    CAS  Article  PubMed  Google Scholar 

  49. Shuster, S. M. (1987). Alternative reproductive behaviors: three discrete male morphs in Paracerceis sculpta, an intertidal isopod from the northern Gulf of California. Journal of Crustacean Biology, 7, 318–327.

    Article  Google Scholar 

  50. Sinervo, B., & Lively, C. M. (1996). The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240–243.

    CAS  Article  Google Scholar 

  51. Spencer, A. M. (1995). Sexual maturity in the male tree weta Hemideina crassidens (Orthoptera: Stenopelmatidae). Wellington, NZ: Victoria University of Wellington.

    Google Scholar 

  52. Zar, J. H. (1999). Biostatistical analysis. Upper Saddle River, NJ: Prentice Hall.

    Google Scholar 

  53. Zelditch, M. L., Swiderski, D. L., Sheets, D. H., & Fink, W. L. (2004). Geometric morphometrics for biologists. San Diego, CA: Academic Press.

    Google Scholar 

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Acknowledgments

We thank Wolf Blanckenhorn and two anonymous referees for valuable comments on the manuscript. This work was supported in part by faculty start-up funds awarded to CDK by Iowa State University and NSF grant DEB-0446758 to DCA.

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Correspondence to Clint D. Kelly.

Appendix

Appendix

See Fig. 6.

Fig. 6
figure6

Scaling relationship for head length (mm) and femur length (mm) in male tree weta for each of the 7 study years. Each morphotype is denoted by differently coloured circles (white 8th instar males; grey 9th instar males and black 10th instar males)

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Kelly, C.D., Adams, D.C. Sexual Selection, Ontogenetic Acceleration, and Hypermorphosis Generates Male Trimorphism in Wellington Tree Weta. Evol Biol 37, 200–209 (2010). https://doi.org/10.1007/s11692-010-9096-1

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Keywords

  • Morphometrics
  • Sexual selection
  • Weaponry
  • Shape
  • Allometry
  • Sexually dimorphism