Evolutionary Biology

, Volume 40, Issue 2, pp 246–260 | Cite as

Becoming Different But Staying Alike: Patterns of Sexual Size and Shape Dimorphism in Bills of Hummingbirds

Research Article

Abstract

Hummingbirds are known for their distinctive patterns of sexual dimorphism, with many species exhibiting sex-related differences in various ecologically-relevant traits, including sex-specific differences in bill shape. It is generally assumed that such patterns are consistent across all hummingbird lineages, yet many taxa remain understudied. In this study we examined patterns of sexual size and sexual shape dimorphism in bills of 32 of 35 species in the monophyletic Mellisugini lineage. We also compared patterns of bill size dimorphism in this group to other hummingbird lineages, using data from 219 hummingbird species. Overall, the presence and degree of sexual size dimorphism was similar across all hummingbird lineages, with the majority of Mellisugini species displaying female-biased sexual size dimorphism, patterns that remain unchanged when analyzed in a phylogenetic context. Surprisingly however, we found that sexual dimorphism in bill shape was nearly absent in the Mellisugini clade, with only 3 of the 32 species examined displaying bill shape dimorphism. Based on observations in other hummingbird lineages, the lack of sexual shape dimorphism in Mellisugini is particularly unusual. We hypothesize that the patterns of sexual size dimorphism observed here may be the consequence of differential selective forces that result from competition for ecological resources. We further propose that an influential mechanism underlying shape dimorphism is competition and niche segregation. Taken together, the evolutionary changes in patterns of sexual shape dimorphism observed in Mellisugini suggest that the evolutionary trends of sexual dimorphism in the Trochilidae are far more dynamic than was previously believed.

Keywords

Sexual dimorphism Geometric morphometrics Sexual size dimorphism Sexual shape dimorphism Hummingbird Mellisugini 

References

  1. Adams, D. C. (2010). Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evolutionary Biology, 10, 1–10.CrossRefGoogle Scholar
  2. Adams, D. C., & Collyer, M. L. (2007). The analysis of character divergence along environmental gradients and other covariates. Evolution, 61, 510–515.PubMedCrossRefGoogle Scholar
  3. Adams, D. C., & Collyer, M. L. (2009). A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution, 63, 1143–1154.PubMedCrossRefGoogle Scholar
  4. Adams, D. C., & Nistri, A. (2010). Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology, 10, 1–10.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. Adams, D. C., West, M. E., & Collyer, M. L. (2007). Location-specific sympatric morphological divergence as a possible response to species interactions in West Virginia Plethodon salamander communities. Journal of Animal Ecology, 76, 289–295.PubMedCrossRefGoogle Scholar
  7. Alves, S. M., & Belo, M. (2002). Morphometric variations in the house fly, Musca domestica (L.) with latitude. Genetica, 115, 243–251.PubMedCrossRefGoogle Scholar
  8. Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.Google Scholar
  9. Andersson, M. (1994). Sexual selection. Princeton, NJ: Princeton University Press.Google Scholar
  10. Berns, C. M., & Adams, D. C. (2010). Bill shape and sexual shape dimorphism between two species of temperate hummingbirds: Black-chinned Hummingbirds (Archilochus alexandri) and Ruby-throated Hummingbirds (Archilochus colubris). The Auk, 127, 626–635.CrossRefGoogle Scholar
  11. Bird, D. M. (2004). The bird almanac: A guide to essential facts and figures of the world’s birds. Firefly Books (U.S.) Inc, Buffalo, NY.Google Scholar
  12. BirdLife International. (2012). IUCN red list for birds. Downloaded from http://www.birdlife.org on 29 May 2012.
  13. Bleiweiss, R. (1992). Reversed plumage ontogeny in a female hummingbird- implications for the evolution of iridescent colors and sexual dimorphism. Biological Journal of the Linnean Society, 47, 183–195.CrossRefGoogle Scholar
  14. Bleiweiss, R. (1997). Covariation of sexual dichromatism and plumage colors in lekking and non-lekking birds: A comparative analysis. Evolutionary Ecology, 11, 217–235.CrossRefGoogle Scholar
  15. Bleiweiss, R. (1998). Origin of hummingbird faunas. Biological Journal of the Linnean Society, 65, 77–97.CrossRefGoogle Scholar
  16. Bleiweiss, R. (1999). Joint effects of feeding and breeding behaviour on trophic dimorphism in hummingbirds. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266, 2491–2497.PubMedCrossRefGoogle Scholar
  17. Bookstein, F. L. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge: Cambridge University Press.Google Scholar
  18. Bookstein, F., Schäfer, K., Prossinger, H., Seidler, H., Fieder, M., Stringer, C., et al. (1999). Comparing frontal cranial profiles in archaic and modern Homo by morphometric analysis. The Anatomical Record, 257, 217–224.PubMedCrossRefGoogle Scholar
  19. Brown, J. H., & Bowers, M. A. (1985). Community organization in hummingbirds: Relationships between morphology and ecology. The Auk, 102, 251–269.CrossRefGoogle Scholar
  20. Butler, M. A., Sawyer, M. A., & Losos, J. B. (2007). Sexual dimorphism and adaptive radiation in Anolis lizards. Nature, 447, 202–205.PubMedCrossRefGoogle Scholar
  21. Butler, M. A., Schoener, T. W., & Losos, J. B. (2000). The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. Evolution, 54, 259–272.PubMedGoogle Scholar
  22. Carpenter, F. L., Hixon, M. A., Paton, D. C., Temeles, E. J., & Russell, R. W. (1991). Sexual differences in resource acquisition by migrant hummingbirds. Acta XX Congressus Internationalis Ornithologici, 2, 1156–1165.Google Scholar
  23. Collins, B. G., & Paton, D. C. (1989). Consequences of differences in body mass, wing length and leg morphology for nectar-feeding birds. Austral Ecology, 14, 269–289.CrossRefGoogle Scholar
  24. Collyer, M. L., & Adams, D. C. (2007). Analysis of two-state multivariate phenotypic change in ecological studies. Ecology, 8, 683–692.CrossRefGoogle Scholar
  25. Colwell, R. K. (2000). Rensch’s Rule crosses the line: convergent allometry of sexual size dimorphism in hummingbirds and flower mites. The American Naturalist, 156, 495–510.CrossRefGoogle Scholar
  26. Darwin, C. R. (1871). The descent of man and selection in relation to sex. London: John Murray.CrossRefGoogle Scholar
  27. Dryden, I. L., & Mardia, K. V. (1993). Multivariate shape analysis. SankhyÄ: The Indian Journal of Statistics, Series A (1961–2002), 55, 460–480.Google Scholar
  28. Dryden, I. L., & Mardia, K. V. (1998). Statistical analysis of shape. Chichester: John Wiley and Sons.Google Scholar
  29. Evans, M. R., Martins, T. L. E., & Haley, M. P. (1995). Inter-sexual and intra-sexual patterns of fluctuating asymmetry in the Red-billed Streamertail- should symmetry always increase with ornament size. Behavioral Ecology and Sociobiology, 37, 15–23.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. Feinsinger, P. (1978). Ecological interactions between plants and hummingbirds in a successional tropical community. Ecological Monographs, 48, 269–287.CrossRefGoogle Scholar
  32. Feinsinger, P., & Colwell, R. K. (1978). Community organization among neotropical nectar-feeding birds. American Zoologist, 18, 779–795.Google Scholar
  33. Garland, T., Dickerman, A. W., Janis, C. M., & Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology, 42, 265–292.Google Scholar
  34. Gunz, P., Mitteroecker, P., & Bookstein, F. (2005). Semi-landmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). New York: Kluwer.CrossRefGoogle Scholar
  35. Hedrick, A. V., & Temeles, E. J. (1989). The evolution of sexual dimorphism in animals: Hypotheses and tests. Trends in Ecology & Evolution, 4, 136.CrossRefGoogle Scholar
  36. Hendry, A. P., Kelly, M. L., Kinnison, M. T., & Reznick, D. L. (2006). Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of guppies. Journal of Evolutionary Biology, 19, 741–754.PubMedCrossRefGoogle Scholar
  37. Jones, A. G., & Ratterman, N. L. (2009). Mate choice and sexual selection: What have we learned since Darwin? Proceedings of the National Academy of Sciences, 106, 10001–10008.CrossRefGoogle Scholar
  38. Kodric-Brown, A., & Brown, J. H. (1978). Influence of economics, interspecific competition, and sexual dimorphism on territoriality of migrant Rufous Hummingbirds. Ecology, 59, 285–296.CrossRefGoogle Scholar
  39. Lovich, J. E., & Gibbons, J. W. (1992). A review of techniques for quantifying sexual size dimorphism. Growth, Development, and Aging, 56, 269–281.PubMedGoogle Scholar
  40. McGuire, J. A., Witt, C. C., Altshuler, D., & Remsen, J. V. (2007). Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. Systematic Biology, 56, 837–856.PubMedCrossRefGoogle Scholar
  41. McGuire, J., Witt, C., Remsen, J., Dudley, R., & Altshuler, D. (2009). A higher-level taxonomy for hummingbirds. Journal of Ornithology, 150, 155–165.CrossRefGoogle Scholar
  42. Potter, K. A., Bose, T., & Yamaguchi, A. (2005). Androgen-induced vocal transformation in adult female African Clawed Frogs. Journal of Neurophysiology, 94, 415–428.PubMedCrossRefGoogle Scholar
  43. R Development Core Team. (2010). R: A language and environment for statistical computing, version 2.11.1 R Foundation for Statistical Computing, Vienna.Google Scholar
  44. Rodríguez-Flores, C. I., & Stiles, G. (2005). Ecomorphological analysis of a community of hermit hummingbirds (Trochilidae, Phaethorninae) and their flowers in Colombian Amazonia. Ornitología Colombiana, 3, 7–27.Google Scholar
  45. Rohlf, F. J. (1999). Shape statistics: Procrustes superimpositions and tangent spaces. Journal of Classification, 16, 197–223.Google Scholar
  46. Rohlf, F. J. (2004). TPSSplin, version 1.20. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
  47. Rohlf, F. J. (2005). TPSRelW, version 1.42. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
  48. Rohlf, F. J. (2010). TPSDig2, version 2.16. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
  49. Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecology & Evolution, 8, 129–132.CrossRefGoogle Scholar
  50. Rohlf, F. J., & Slice, D. E. (1990). Extentions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.CrossRefGoogle Scholar
  51. Selander, R. K. (1972). Sexual selection and dimorphism in birds. In B. G. Campbell (Ed.), Sexual Selection and the descent of man (1871–1971) (pp. 180–230). Chicago, IL: Aldine.Google Scholar
  52. Serb, J. M., Alejandrino, A., Otárola-Castillo, E., & Adams, D. C. (2011). Morphological convergence of shell shape in distantly related scallop species (Mollusca: Pectinidae). Zoological Journal of the Linnean Society, 163, 571–584.CrossRefGoogle Scholar
  53. Slatkin, M. (1984). Ecological causes of sexual dimorphism. Evolution, 38, 622–630.CrossRefGoogle Scholar
  54. Stephens, P. R., & Wiens, J. J. (2009). Evolution of sexual size dimorphism in emydid turtles: Ecological dimorphism, Rensch’s Rule, and sympatric divergence. Evolution, 63, 910–925.PubMedCrossRefGoogle Scholar
  55. Stiles, F. G. (1983). Systematics of the southern forms of Selasphorus (Trochilidae). The Auk, 100, 311–325.Google Scholar
  56. Stiles, F. G. (1995). Behavioral, ecological and morphological correlates of foraging for arthropods by the hummingbirds of a tropical wet forest. The Condor, 97, 853–878.CrossRefGoogle Scholar
  57. Stuart-Fox, D. M., & Ord, T. J. (2004). Sexual selection, natural selection and the evolution of dimorphic coloration and ornamentation in agamid lizards. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271, 2249–2255.PubMedCrossRefGoogle Scholar
  58. Temeles, E. J., Goldman, R. S., Kudla, A. U., & Stouffer, P. C. (2005). Foraging and territory economics of sexually dimorphic Purple-throated Caribs (Eulampis jugularis) on three Heliconia morphs. The Auk, 122, 187–204.CrossRefGoogle Scholar
  59. Temeles, E. J., & Kress, W. J. (2003). Adaptation in a plant-hummingbird association. Science, 300, 630–633.PubMedCrossRefGoogle Scholar
  60. Temeles, E. J., Miller, J. S., & Rifkin, J. L. (2010). Evolution of sexual dimorphism in bill size and shape of hermit hummingbirds (Phaethornithinae): A role for ecological causation. Philosophical Transactions of the Royal Society B: Biological Sciences, 365, 1053–1063.CrossRefGoogle Scholar
  61. Temeles, E. J., & Roberts, W. M. (1993). Effect of sexual dimorphism in bill length on foraging behavior: An experimental analysis of hummingbirds. Oecologia, 94, 87–94.CrossRefGoogle Scholar
  62. Wood, G. L. (Ed.). (1983). Guinness book of animal facts and feats. New York: Sterling Publishing Co Inc.Google Scholar
  63. Worthington, A. M., Berns, C. M., & Swallow, J. G. (2012). Size matters, but so does shape: Quantifying complex shape changes in a sexually selected trait in stalk-eyed flies (Diptera: Diopsidae). Biological Journal of the Linnaean Society, 106, 104–113.CrossRefGoogle Scholar
  64. Zusi, R. L., & Gill, F. B. (2009). The marvelous tail of Loddigesia mirabilis (Trochilidae). The Auk, 126, 590–603.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.Department of Ecology, Evolution and Organismal BiologyIowa State UniversityAmesUSA

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