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

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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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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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