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

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.

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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, 1–10.

    Article  Google Scholar 

  2. Adams, D. C., & Collyer, M. L. (2007). The analysis of character divergence along environmental gradients and other covariates. Evolution, 61, 510–515.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    PubMed  Article  Google Scholar 

  7. Alves, S. M., & Belo, M. (2002). Morphometric variations in the house fly, Musca domestica (L.) with latitude. Genetica, 115, 243–251.

    PubMed  Article  Google 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.

    Article  Google 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.

  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.

    Article  Google 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.

    Article  Google Scholar 

  15. Bleiweiss, R. (1998). Origin of hummingbird faunas. Biological Journal of the Linnean Society, 65, 77–97.

    Article  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google Scholar 

  19. Brown, J. H., & Bowers, M. A. (1985). Community organization in hummingbirds: Relationships between morphology and ecology. The Auk, 102, 251–269.

    Article  Google Scholar 

  20. Butler, M. A., Sawyer, M. A., & Losos, J. B. (2007). Sexual dimorphism and adaptive radiation in Anolis lizards. Nature, 447, 202–205.

    PubMed  Article  CAS  Google 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.

    PubMed  CAS  Google 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.

    Article  Google Scholar 

  24. Collyer, M. L., & Adams, D. C. (2007). Analysis of two-state multivariate phenotypic change in ecological studies. Ecology, 8, 683–692.

    Article  Google 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.

    Article  Google Scholar 

  26. Darwin, C. R. (1871). The descent of man and selection in relation to sex. London: John Murray.

    Google 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.

  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.

    Article  Google 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.

    Article  Google Scholar 

  31. Feinsinger, P. (1978). Ecological interactions between plants and hummingbirds in a successional tropical community. Ecological Monographs, 48, 269–287.

    Article  Google 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.

    Google 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.

    Article  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  CAS  Google 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.

    Article  Google 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.

    PubMed  CAS  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  Google 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.

    PubMed  Article  Google 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.

  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.

  47. Rohlf, F. J. (2005). TPSRelW, version 1.42. Department of Ecology and Evolution, State University of New York, Stony Brook.

  48. Rohlf, F. J. (2010). TPSDig2, version 2.16. Department of Ecology and Evolution, State University of New York, Stony Brook.

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

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  53. Slatkin, M. (1984). Ecological causes of sexual dimorphism. Evolution, 38, 622–630.

    Article  Google 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.

    PubMed  Article  Google 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.

    Article  Google 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.

    PubMed  Article  Google 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.

    Article  Google Scholar 

  59. Temeles, E. J., & Kress, W. J. (2003). Adaptation in a plant-hummingbird association. Science, 300, 630–633.

    PubMed  Article  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  64. Zusi, R. L., & Gill, F. B. (2009). The marvelous tail of Loddigesia mirabilis (Trochilidae). The Auk, 126, 590–603.

    Article  Google Scholar 

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Acknowledgments

We thank S.M. Binz, M.B. Manes, A.W. Worthington, N.M. Valenzuela, A.N. Pairett, A. Alejandrino, A.J. Krause, A. Kraemer, R. Literman, Badenhorst, G. Rivera, A. Kaliontzopoulou, J.M. Serb, N.A. Gidaszewski, N. Navarro, and one anonymous reviewer for comments, and E.J. Temeles, R.M. Zink, A. Cardini and one anonymous reviewer made valuable suggestions on previous versions of the manuscript. We thank the United States National Science Foundation for partial financial support through grants DEB-1118884 (to DCA) and National Science Foundation Graduate Research Fellowship DGE0751279 (to CMB), the Society for the Study of Evolution Rosemary Grant Award (to CMB) and American Museum of Natural History Collections Grant (to CMB). Finally, we thank the many institutions (standard abbreviation given in parentheses), curators and collection managers who provided specimens, especially P. Sweet and G. Barrowclough (AMNH), S. Rogers (CM), C. Dardia and K. Botswick (CUMV), J. Woods (DMNH), D. Willard (FMNH), K. Garrett (LACM), J. Trimble (MCZ), C. Witt (MSB), C. Cicero (MVZ), P. Unitt (SDNHM), J. Hinshaw (UMMZ), C. Angle and D. James (NMNH), R. Corado (WFVZ), and K. Zyskowski (YPM), and K. Roe (NHM at ISU).

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Correspondence to Chelsea M. Berns.

Appendices

Appendix

See Tables 3 and 4.

Table 3 Number of males and females in each species of the 32 hummingbirds in the Mellisugini clade with the sexual size dimorphism ratio (negative numbers indicate male-biased SSD) and magnitude of sexual shape dimorphism
Table 4 Species sexual size dimorphism ratios from literature (negative numbers indicate male-biased SSD)

Specimens Examined to Quantify Morphological Variation

We examined the left lateral side of bills from collections at Carnegie Museum of Natural History (CM), Cornell University Museum of Vertebrates (CUMV), Delaware Museum of Natural History (DMNH), Field Museum of Natural History (FMNH), Los Angeles County Museum (LACM), Museum of Comparative Zoology (MCZ), Museum of Southwestern Biology (MSB), Museum of Vertebrate Zoology (MVZ), San Diego Natural History Museum (SDNHM), University of Michigan Museum of Zoology (UMMZ), National Museum of Natural History (NMNH), Western Foundation of Vertebrate Zoology (WFVZ), and Yale Peabody Museum (YPM). Specific specimens, listed by institution, include the following:

AMNH: 100678, 109537, 117704, 124278, 124279, 124280, 124281, 13002, 131195, 145839, 151434, 151437, 151458, 151459, 170352, 171148, 171149, 171157, 179065, 181241, 182361, 229094, 234478, 235492, 235680, 235859, 305591, 305592, 229094, 234478, 235492, 235680, 235859, 305591, 305592, 326286, 326287, 326290, 326292, 326293, 326295, 326296, 361892, 361894, 337924,61896, 361897, 361898, 37784, 37893, 37894, 37896, 37903, 37905, 37911, 37938, 37941, 37945, 37947, 37949, 37950, 37952, 37953, 37957, 37981, 38004, 38715, 389741, 394200, 394202, 394204, 394206, 394208, 394215, 394217, 394218, 394219, 394220, 394222, 437741, 46310, 46608, 46631, 46634, 46636, 46637, 46655, 46659, 46713, 46736, 484400, 484402, 484403, 484407, 484408, 484409, 484525, 484529, 484547, 484550, 484551, 484553, 484554, 484555, 484564, 484580, 484597, 484598, 484599, 484600, 484601, 484602, 484603, 484607, 484613, 484620, 484628, 484629, 484630, 484631, 484632, 484710, 484791, 484794, 484802, 484817, 484818, 484821, 484824, 484826, 484828, 484829, 484831, 484832, 484833, 484836, 484837, 484838, 484840, 484841, 484842, 484842, 484843, s484845, 484846, 484850, 484872, 484929, 484930, 484935, 484938, 484945, 484948, 484949, 484950, 484951, 484956, 484958, 484960, 484984, 484986, 484988, 54154, 60746, 71312, 73093, 73094, 78956, 793430, 806281, 812050, 824739, 99115, 99116.

CM: 67643, 101705, 101706, 113457, 113462, 124330, 125660, 125728, 128495, 138725, 142822, 142892, 155017, 158840, 159356, 159357, 159358, 159359, 159389, 159362, 159365, 159390, 159391, 162238, 162240, 162248, 19584, 19585, 19586, 19587, 19586, 19587, 19588, 19601, 19602, 19603, 19604, 19605, 19608, 19609, 19647, 19648, 19650, 19651, 19655, 19662, 19666, 19671, 19675, 19676, 19680, 19681, 19688, 19689, 19694, 19695, 19696, 19698, 19699, 19707, 19708, 19709, 19710, 19712, 19713, 19714, 28207, 29271, 29322, 30567, 30574, 30591, 30765, 30811, 30838, 30847, 30854, 30861, 30854, 30861, 30862, 30970, 31079, 31087, 33480, 33974, 34185, 34186, 34206, 34207, 34209, 34210, 34213, 34224, 34261, 48058, 81925, 81939, 95191, 106686, 106837, 119903, 119978, 120388, 135818, 141455, 141457, 141465, 141466, 142891, 142893, 143338, 144792, 144797, 35046, 37817, 37863, 37869, 37870, 37871, 37872, 41264, 42503, 42504, 43719, 51309, 51310, 79155, 79156, 79159, 80549, 85050, 85320, 85465, 85498, 85499 125705, 125706, 125710, 141875, 142477, 151407, 152912, 153151, 153802, 154036, 154146, 154621, 158828, 1588289, 158830, 158831, 158832, 158833, 158834, 158836, 158837, 159323, 159324, 159325, 159327, 159328, 159329, 159330, 159331, 159332, 159333, 159334, 159335, 159336, 159337, 159338, 159339, 159340, 159342, 159343, 159345, 159346, 159347, 159348, 159349, 159350, 166922, 167457, 168761, 169649, 170846, 170867, 95217.

CUMV: 12030, 5428 14986, 21604, 23717, 24397, 37009, 44079, 44128, 44129, 44130, 44131, 44171, 49013, 50001, 50780, 51239, 5352, 5355, 5357, 5358, 5361, 5362, 5363, 5364, 5365, 5367, 5382.

DMNH: 6273, 12401, 12402, 12403, 12404, 12405, 18677, 18678, 18679, 18681, 18685, 22409, 22419, 22423, 24683, 24687, 24690, 24691, 24692, 24693, 24694, 24695, 24696, 24697, 24698, 24700, 24701, 24702, 24704, 24705, 24706, 24709, 59797, 59813, 59814, 59815 1400, 1426, 1436, 19019, 19025, 59806.

FMNH: 138884, 138887, 42934, 120625, 12692, 1279, 1280, 1281, 1283, 1284, 138877, 138879, 138882, 138883, 138885, 138888, 179490, 179491, 179494, 186014, 186015, 186016, 207017, 207019, 207024, 207028, 207029, 207030, 207031, 207032, 207033, 207035, 207036, 207037, 207038, 207039, 207040, 207041, 207043, 208746, 208747, 208748, 208749, 208750, 215969, 21940, 24234, 24235, 275613, 285092, 285093, 285094, 293745, 299872, 302753, 32014, 36108, 36113, 36610, 372482, 372483, 372485, 372486, 42822, 42824, 42826, 42931, 42932, 42935, 45528, 45549, 45550, 46407, 46410, 46411, 46417, 46419, 46420, 46461, 46462, 46463, 47104, 47106, 47108, 47109, 47111, 53307, 53873, 56771, 56773, 56774, 61598, 61599, 61714, 61715, 61716, 61719, 61720, 65515, 65517, 65519, 66328, 67764, 67767, 67769, 67770, 67771, 72207, 72209, 72212, 72213, 91943, 91944, 138705, 138720, 138723, 138725, 14653, 14654, 14655, 14656, 14657, 14658, 14659, 14661, 14662, 14663, 14666, 14667, 14668, 14670, 14672, 14673, 14674, 14675, 14676, 14678, 159838, 159839, 161019, 16575, 16576, 93036, 93037, 93038, 93039, 93040.

LACM: 14115, 15187, 15641, 15643, 15645, 21992, 24216, 24218, 24453, 32465, 32467, 3377, 4521, 50712, 6529, 6530, 6596, 73865, 73867, 77860, 78165, 103469, 107665, 111607, 111608, 14107, 15560, 15562, 15563, 15565, 15566, 15642, 15644, 15646, 15646, 15647, 15649, 15650, 15651, 1766, 1793, 18004, 18381, 19821, 21993, 21994, 2416, 2417, 2423, 2424, 2426, 25430, 25432, 25434, 25435, 3045, 3046, 3047, 3048, 3051, 3053, 3055, 3072, 3128, 3129, 3130, 3204, 32466, 32468, 4069, 85325, 85326, 14127, 14138, 14139, 1927, 3381, 78618, 78619, 78621, 78623, 78624, 78625, 78626, 78627, 78632, 78643, 78646, 78652, 78653, 78654, 78656, 78659, 78661, 78662, 78663, 78664, 78668, 78669, 78671, 78677, 78678, 78683, 78684, 78688, 78691, 78694.

LSU: 91976, 143500, 143507, 143510, 35139, 64031, 64032, 64033.

MCZ: 100182, 103286, 100182, 103286.

MSB: 14801, 22663, 22665, 22668, 22670, 22671, 22677.

MVZ: 138272, 138273, 109221, 110077, 110078, 110079, 110080, 11860, 139415, 139415, 139417, 139418, 153271, 153272, 156457, 157758, 157759, 160840, 163525, 107024, 116741, 12811, 19920, 19921, 19922, 19923, 19925, 22484, 22704, 26729, 26730, 27927, 27928, 27929, 27930, 27931, 3192, 3194, 3197, 32864, 32870, 32875, 32878, 32880, 32881, 32882, 32883, 32884, 32887, 32888, 32889, 32900, 32903, 3655, 3698, 3700, 3785, 40727, 40728, 40731, 41534, 41927, 4194, 4195, 43242, 45343, 5249, 77338, 80946.

NMNH: 233774, 101885, 101886, 103295, 108743, 117267, 127670, 127671, 128173, 130564, 131574, 132865, 134348, 134353, 140265, 140275, 140281, 140316, 140331, 142249, 149468, 149470, 149482, 149486, 149489, 149490, 149492, 149495, 149497, 150791, 152545, 154785, 154787, 154791, 154792, 154793, 154820, 162635, 170608, 170656, 174575, 174579, 174583, 174585, 174586, 174587, 174589, 174590, 174592, 174594, 174596, 174597, 174599, 174600, 174603, 174604, 174605, 174619, 174627, 184077, 189789, 190522, 190524, 190525, 190526, 190527, 190972, 200318, 200319, 200322, 200324, 201116, 201118, 201122, 201123, 201125, 201126, 204617, 208257, 220663, 233773, 233775, 233776, 236667, 24624, 24625, 24626, 24627, 253389, 253390, 253723, 263880, 263881, 263882, 263883, 264509, 264759, 273932, 274230, 274236, 277269, 287983, 2896, 30274, 309063, 309718, 309720, 309722, 309723, 309777, 309879, 317261, 32048, 327689, 333521, 349574, 35175, 352823, 352824, 375720, 375722, 386974, 386975, 386976, 386977, 386978, 386979, 386980, 389269, 392260, 392262, 392264, 392265, 392270, 392271, 392271, 401554, 401554, 401556, 401557, 41473, 41475, 44741, 453719, 453720, 453723, 453725, 453726, 453727, 453735, 453736, 453739, 453740, 456067, 456069, 456475, 45863, 462930, 462937, 47183, 50278, 52295, 52297, 52298, 54321, 543863, 55964, 573638, 60088, 6054, 6058, 627430, 74023, 74659, 74662, 74665, 74665, 74666, 74668, 84137, 84221, 86348, 90369, 92045, 99368, 99513, 108369, 117258, 117269, 129247, 129249, 129250, 129252, 129257, 134343, 140254, 140255, 140256, 140257, 140258, 140259, 140266, 168422, 203268, 234334, 235077, 235074, 258387, 467031, 589963, 91738, 91740, 94957, 91959.

SDNHM: 12411, 12423, 12436, 15648, 15794, 15828, 15860, 15860, 15924, 17485, 17488, 17842, 19265, 22427, 22428, 22429, 22430, 22431, 22432, 22433, 22434, 31503, 31504, 3196, 3197, 36032, 36033, 43552, 469, 50045, 50616, 51785, 9286, 9492, 9753, 17251, 22386, 22387, 22389, 22463, 30108, 30417, 449, 450.

UMMZ: 126341, 126344, 126345, 126347, 126348, 126350, 126373, 126374, 126376, 126377, 126378, 126382, 126383, 126425, 126432, 126434, 132424, 132425, 132426, 132428, 150182, 164649, 164662, 164664, 164667, 164668, 164669, 215480, 27469, 60462, 62719, 62721, 65094, 98235, 100160, 111051, 111052, 111054, 119549, 126351, 126424, 126428, 126429, 134979, 27465, 49777, 92163, 111820, 113646, 113649, 126291, 126292, 126294, 126295, 126296, 126297, 126299, 126300, 126301, 126301, 126302, 126303, 126304, 126306, 126307, 126310, 126314, 134697, 136434, 156250, 164455, 164461, 164463, 164468, 164470, 164471, 164472, 164473, 164474, 164490, 164491, 164492, 164492, 164496, 164498, 164500, 164501, 164502, 164504, 164505, 164506, 164507, 164508, 164509, 164510, 164514, 164515, 164517, 164518, 164519, 164525, 164526, 164527, 164528, 164529, 164530, 199030, 199031, 213109, 213110, 221599, 221794, 224043, 231028, 231029, 236468, 238200, 239425, 239499, 239601, 239604, 239631, 240778, 240967, 241265, 241283, 31639, 52980, 55809, 62710, 62711, 62713, 62714, 67020, 71337, 74542, 90352.

WFVZ: 19187, 19188, 19192, 21786, 21787, 21790, 21796, 21797, 21849, 21850, 25450, 34005, 34006, 39248, 39249, 39250, 39252, 39253, 39254, 48247, 49304, 50642, 8539, 8540, 10119, 1515, 1516, 1517, 21798, 21803, 21804, 21806, 21809, 2714, 32155, 32156, 49304, 49308.

YPM: 6442, 99650.

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Berns, C.M., Adams, D.C. Becoming Different But Staying Alike: Patterns of Sexual Size and Shape Dimorphism in Bills of Hummingbirds. Evol Biol 40, 246–260 (2013). https://doi.org/10.1007/s11692-012-9206-3

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Keywords

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