How traits affect speciation is a long-standing question in evolution. We investigate whether speciation rates are affected by the traits themselves or by the rates of their evolution, in hummingbirds, a clade with great variation in speciation rates, morphology and ecological niches. Further, we test two opposing hypotheses, postulating that speciation rates are promoted by trait conservatism or, alternatively, by trait divergence. To address these questions, we analyse morphological (body mass and bill length) and niche traits (temperature and precipitation position and breadth, and mid-elevation), using a variety of methods to estimate speciation rates and correlate them with traits and their evolutionary rates. When it comes to the traits, we find faster speciation in smaller hummingbirds with shorter bills, living at higher elevations and experiencing greater temperature ranges. As for the trait evolutionary rates, we find that speciation increases with rates of divergence in the niche traits, but not in the morphological traits. Together, these results reveal the interplay of mechanisms through which different traits and their evolutionary rates (conservatism or divergence) influence the origination of hummingbird diversity.

Center for Theoretical Study Charles University and the Czech Academy of Science Jilska 1 11000 Prague Czechia

Consortium for Inter Disciplinary Environmental Research Stony Brook University 129 Dana Hall Stony Brook NY 11794 USA

Departamento de Ecologia Universidade Federal de Goiás Campus Samambaia Goiânia Goiás Brazil

Department of Ecology and Evolution Stony Brook University 650 Life Sciences Building Stony Brook NY 11794 USA

Department of Ecology Charles University Vinicna 7 12844 Prague Czechia

Department of Natural Sciences and Mathematics Pontificia Universidad Javeriana Cali Cl 18 118 250 Cali Valle del Cauca Colombia

Swiss Federal Institute for Forest Snow and Landscape Research WSL Zürcherstrasse 111 8903 Birmensdorf Switzerland

Villum Center for Global Mountain Biodiversity and Center for Macroecology Evolution and Climate GLOBE Institute University of Copenhagen Universitetsparken 15 2100 Copenhagen Denmark

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Simpson GG. 1953. The major features of evolution. New York, NY: Columbia University Press.

Wiens JJ. 2017. What explains patterns of biodiversity across the Tree of Life? New research is revealing the causes of the dramatic variation in species numbers across branches of the Tree of Life. Bioessays 39, 1-10. (10.1002/bies.201600128) PubMed DOI

Owens IPF, Bennett PM, Harvey PH. 1999. Species richness among birds: body size, life history, sexual selection or ecology? Proc. R. Soc. B 266, 933-939. (10.1098/rspb.1999.0726) DOI

Rolland J, Salamin N. 2016. Niche width impacts vertebrate diversification. Global Ecol. Biogeogr. 25, 1252-1263. (10.1111/geb.12482) DOI

Adams DC, Berns CM, Kozak KH, Wiens JJ. 2009. Are rates of species diversification correlated with rates of morphological evolution? Proc. R. Soc. B 276, 2729-2738. (10.1098/rspb.2009.0543) PubMed DOI PMC

Kozak KH, Wiens JJ. 2010. Accelerated rates of climatic-niche evolution underlie rapid species diversification. Ecol. Lett. 13, 1378-1389. (10.1111/j.1461-0248.2010.01530.x) PubMed DOI

Wiens JJ. 2004. Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution 58, 193-197. PubMed

Calder WA. 1994. When do hummingbirds use torpor in nature? Physiol. Zool. 67, 1051-1076.

Bribiesca R, Herrera-Alsina L, Ruiz-Sanchez E, Sánchez-González LA, Schondube JE. 2019. Body mass as a supertrait linked to abundance and behavioral dominance in hummingbirds: a phylogenetic approach. Ecol. Evol. 9, 1623-1637. (10.1002/ece3.4785) PubMed DOI PMC

Shankar A, Powers DR, Dávalos LM, Graham CH. 2020. The allometry of daily energy expenditure in hummingbirds: an energy budget approach. J. Anim. Ecol. 89, 1254-1261. (10.1111/1365-2656.13185) PubMed DOI

Gittleman JL, Purvis A. 1998. Body size and species-richness in carnivores and primates. Proc. R. Soc. Lond. B 265, 113-119. (10.1098/rspb.1998.0271) PubMed DOI PMC

Feldman A, Sabath N, Pyron RA, Mayrose I, Meiri S. 2016. Body sizes and diversification rates of lizards, snakes, amphisbaenians and the tuatara. Global Ecol. Biogeogr. 25, 187-197. (10.1111/geb.12398) DOI

Feinsinger P, Colwell R. 1978. Community organization among neotropical nectar-feeding birds. Am. Zool. 18, 779-795. (10.1093/icb/18.4.779) DOI

Weinstein BG, Graham CH. 2017. Persistent bill and corolla matching despite shifting temporal resources in tropical hummingbirdplant interactions. Ecol. Lett. 20, 326-335. (10.1111/ele.12730) PubMed DOI

Rico-Guevara A, Rubega MA, Hurme KJ, Dudley R. 2019. Shifting paradigms in the mechanics of nectar extraction and hummingbird bill morphology. Integr. Organismal Biol. 1, oby006. (10.1093/iob/oby006) PubMed DOI PMC

Maglianesi MA, Blüthgen N, Böhning-Gaese K, Schleuning M. 2014. Morphological traits determine specialization and resource use in plant–hummingbird networks in the neotropics. Ecology 95, 3325-3334. (10.1890/13-2261.1) DOI

Dalsgaard B, et al. 2021. The influence of biogeographical and evolutionary histories on morphological trait-matching and resource specialization in mutualistic hummingbird–plant networks. Funct. Ecol. 35, 1120-1133. (10.1111/1365-2435.13784) DOI

Machac A. 2020. The dynamics of bird diversity in the new world. Syst. Biol. 69, 1180-1199. (10.1093/sysbio/syaa028) PubMed DOI PMC

Gómez-Rodríguez C, Baselga A, Wiens JJ. 2015. Is diversification rate related to climatic niche width? Global Ecol. Biogeogr. 24, 383-395. (10.1111/geb.12229) DOI

Sexton JP, Montiel J, Shay JE, Stephens MR, Slatyer RA. 2017. Evolution of ecological niche breadth. Annu. Rev. Ecol. Evol. Syst. 48, 183-206. (10.1146/annurev-ecolsys-110316-023003) DOI

Gaston KJ. 2003. The structure and dynamics of geographic ranges. New York, NY: Oxford University Press.

Slatyer RA, Hirst M, Sexton JP. 2013. Niche breadth predicts geographical range size: a general ecological pattern. Ecol. Lett. 16, 1104-1114. (10.1111/ele.12140) PubMed DOI

Quintero I, Jetz W. 2018. Global elevational diversity and diversification of birds. Nature 555, 246-250. (10.1038/nature25794) PubMed DOI

Bleiweiss R. 1998. Slow rate of molecular evolution in high-elevation hummingbirds. Proc. Natl Acad. Sci. USA 95, 612-616. (10.1073/pnas.95.2.612) PubMed DOI PMC

Li P, Wiens JJ. 2022. What drives diversification? Range expansion tops climate, life history, habitat and size in lizards and snakes. J. Biogeogr. 49, 237-247. (10.1111/jbi.14304) DOI

Wiens JJ, Graham CH. 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Ann. Rev. Ecol. Evol. Syst. 36, 519-539. (10.1007/s00408-009-9147-5) DOI

Vermeji GJ. 1973. Adaptation, versatility, and evolution. Syst. Zool. 22, 466-477.

Schluter D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16, 372-380. PubMed

Cooney CR, Seddon N, Tobias JA. 2016. Widespread correlations between climatic niche evolution and species diversification in birds. J. Anim. Ecol. 85, 869-878. (10.1111/1365-2656.12530) PubMed DOI

Seeholzer GF, Claramunt S, Brumfield RT. 2017. Niche evolution and diversification in a Neotropical radiation of birds (Aves: Furnariidae). Evolution 71, 702-715. (10.1111/evo.13177) PubMed DOI

Schluter D, Pennell MW. 2017. Speciation gradients and the distribution of biodiversity. Nature 546, 48-55. (10.1038/nature22897) PubMed DOI

Rundell RJ, Price TD. 2009. Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol. Evol. 24, 394-399. (10.1016/j.tree.2009.02.007) PubMed DOI

Altshuler DL, Dudley R. 2002. The ecological and evolutionary interface of hummingbird flight physiology. J. Exp. Biol. 205, 2325-2336. (10.1242/jeb.205.16.2325) PubMed DOI

McGuire JA, Witt CC, Remsen JV, Corl A, Rabosky DL, Altshuler DL, Dudley R. 2014. Molecular phylogenetics and the diversification of hummingbirds. Curr. Biol. 24, 910-916. (10.1016/j.cub.2014.03.016) PubMed DOI

Rabosky DL. 2014. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543. (10.1371/journal.pone.0089543) PubMed DOI PMC

Title PO, Rabosky DL. 2019. Tip rates, phylogenies and diversification: what are we estimating, and how good are the estimates? Methods Ecol. Evol. 10, 821-834. (10.1111/2041-210X.13153) DOI

Tobias JA, et al. 2022. AVONET: morphological, ecological and geographical data for all birds. Ecol. Lett. 25, 581-597. (10.1111/ele.13898) PubMed DOI

Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO. 2012. The global diversity of birds in space and time. Nature 491, 444-448. (10.1038/nature11631) PubMed DOI

Revell LJ. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. (10.1111/j.2041-210X.2011.00169.x) DOI

Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza RW, Zimmermann NE, Linder HP, Kessler M. 2017. Climatologies at high resolution for the earth's land surface areas. Sci. Data 4, 1-20. (10.1038/sdata.2017.122) PubMed DOI PMC

Hijmans RJ. 2016. raster: Geographic data analysis and modeling. R package version 2.5-8. See https://cran.r-project.org/package=raster.

BirdLife International and Natureserve. 2015. Bird species distribution maps of the world, version 5.0. Cambridge, UK: Birdlife International.

Ellis-Soto D, Merow C, Amatulli G, Parra JL, Jetz W. 2021. Continental-scale 1km hummingbird diversity derived from fusing point records with lateral and elevational expert information. Ecography 44, 640-652. (10.1111/ecog.05119) DOI

Maliet O, Hartig F, Morlon H. 2019. A model with many small shifts for estimating species-specific diversification rates. Nat. Ecol. Evol. 3, 1086-1092. (10.1038/s41559-019-0908-0) PubMed DOI

Maliet O, Morlon H. 2022. Fast and accurate estimation of species-specific diversification rates using data augmentation. Syst. Biol. 71, 353-366. (10.1093/sysbio/syab055) PubMed DOI

Moore BR, Höhna S, May MR, Rannala B, Huelsenbeck JP. 2016. Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures. Proc. Natl Acad. Sci. USA 113, 201518659. (10.1073/pnas.1518659113) PubMed DOI PMC

Louca S, Pennell MW. 2020. Extant timetrees are consistent with a myriad of diversification histories. Nature 580, 501-505. (10.1038/s41586-020-2176-1) PubMed DOI

Cooney CR, Thomas GH. 2021. Heterogeneous relationships between rates of speciation and body size evolution across vertebrate clades. Nat. Ecol. Evol. 5, 101-110. (10.1038/s41559-020-01321-y) PubMed DOI

Rabosky DL, Grundler M, Anderson C, Title P, Shi JJ, Brown JW, Huang H, Larson JG. 2014. BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5, 701-707. (10.1111/2041-210X.12199) DOI

Gill F, Donsker D, Rasmussen P. 2022. IOC World Bird List (v12.2). (10.14344/IOC.ML.12.1) DOI

Rabosky DL, Huang H. 2016. A robust semi-parametric test for detecting trait-dependent diversification. Syst. Biol. 65, 181-193. (10.1093/sysbio/syv066) PubMed DOI

Harvey MG, Rabosky DL. 2018. Continuous traits and speciation rates: alternatives to state-dependent diversification models. Methods Ecol. Evol. 9, 984-993. (10.1111/2041-210X.12949) DOI

Pagel M. 1999. Inferring the historical patterns of biological evolution. Nature 401, 877-884. (10.1038/44766) PubMed DOI

Pennell MW, Eastman JM, Slater GJ, Brown JW, Uyeda JC, FitzJohn RG, Alfaro ME, Harmon LJ. 2014. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 30, 2216-2218. (10.1093/bioinformatics/btu181) PubMed DOI

Beltrán DF, Shultz AJ, Parra JL. 2021. Speciation rates are positively correlated with the rate of plumage color evolution in hummingbirds. Evolution 75, 1665-1680. (10.1111/evo.14277) PubMed DOI

Rojas D, Jo M, Pereira R, Fonseca C. 2018. Corrigendum to: eating down the food chain: generalism is not an evolutionary dead end for herbivores (Ecology Letters, (2018), 21, 3, (402–410), 10.1111/ele.12911). Ecol. Lett. 21, 1124-1126. (10.1111/ele.12968) PubMed DOI

Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W. 2018. caper: Comparative Analyses of Phylogenetics and Evolution in R.

Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1-22. (10.18637/jss.v033.i02) PubMed DOI

Dormann CF, et al. 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27-46. (10.1111/j.1600-0587.2012.07348.x) DOI

Title PO, Burns KJ. 2015. Rates of climatic niche evolution are correlated with species richness in a large and ecologically diverse radiation of songbirds. Ecol. Lett. 18, 433-440. (10.1111/ele.12422) PubMed DOI

Phillimore AB, Freckleton RP, Orme CDL, Owens IPF. 2006. Ecology predicts large-scale patterns of phylogenetic diversification in birds. Am. Nat. 168, 220-229. (10.1086/505763) PubMed DOI

Sayol F, Lapiedra O, Ducatez S, Sol D. 2019. Larger brains spur species diversification in birds. Evolution 73, 2085-2093. (10.1111/evo.13811) PubMed DOI

Claramunt S, Derryberry EP, Remsen JV, Brumfield RT. 2012. High dispersal ability inhibits speciation in a continental radiation of passerine birds. Proc. R. Soc. B 279, 1567-1574. (10.1098/rspb.2011.1922) PubMed DOI PMC

Rodríguez-Flores CI, Ornelas JF, Wethington S, Arizmendi M. 2019. Are hummingbirds generalists or specialists? Using network analysis to explore the mechanisms influencing their interaction with nectar resources. PLoS ONE 14, e0211855. (10.1371/journal.pone.0211855) PubMed DOI PMC

Dellinger AS, Pérez-Barrales R, Michelangeli FA, Penneys DS, Fernández-Fernández DM, Schönenberger J. 2021. Low bee visitation rates explain pollinator shifts to vertebrates in tropical mountains. New Phytol. 231, 864-877. (10.1111/nph.17390) PubMed DOI

Castellanos MC, Wilson P, Thomson JD. 2004. ‘Anti-bee’ and ‘pro-bird’ changes during the evolution of hummingbird pollination in Penstemon flowers. J. Evol. Biol. 17, 876-885. (10.1111/j.1420-9101.2004.00729.x) PubMed DOI

Graham CH, Parra JL, Rahbek C, McGuire JA. 2009. Phylogenetic structure in tropical hummingbird communities. Proc. Natl Acad. Sci. USA 106, 19 673-19 678. (10.1073/pnas.0901649106) PubMed DOI PMC

Pérez-Escobar OA, et al. 2022. The Andes through time: evolution and distribution of Andean floras. Trends Plant Sci. 27, 364-378. (10.1016/j.tplants.2021.09.010) PubMed DOI

Chaves JA, Weir JT, Smith TB. 2011. Diversification in Adelomyia hummingbirds follows Andean uplift. Mol. Ecol. 20, 4564-4576. (10.1111/j.1365-294X.2011.05304.x) PubMed DOI

Castro-Insua A, Gómez-Rodríguez C, Wiens JJ, Baselga A. 2018. Climatic niche divergence drives patterns of diversification and richness among mammal families. Sci. Rep. 8, 8781. (10.1038/s41598-018-27068-y) PubMed DOI PMC

Moen DS, Wiens JJ. 2017. Microhabitat and climatic niche change explain patterns of diversification among frog families. Am. Nat. 190, 29-44. (10.1086/692065) PubMed DOI

Rabosky DL, Santini F, Eastman J, Smith SA, Sidlauskas B, Chang J, Alfaro ME. 2013. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat. Commun. 4, 1-8. (10.1038/ncomms2958) PubMed DOI

Bleiweiss R. 1998. Tempo and mode of hummingbird evolution. Biol. J. Linnean Soc. 65, 63-76. (10.1006/bijl.1998.0241) DOI

Crouch NMA, Ricklefs RE. 2019. Speciation rate is independent of the rate of evolution of morphological size, shape, and absolute morphological specialization in a large clade of birds. Am. Nat. 193, 78-91. (10.1086/701630) PubMed DOI

Crouch NMA, Tobias JA. 2022. The causes and ecological context of rapid morphological evolution in birds. Ecol. Lett. 25, 611-623. (10.1111/ele.13962) PubMed DOI

Rabosky DL. 2010. Extinction rates should not be estimated from molecular phylogenies. Evolution 64, 1816-1824. (10.1111/j.1558-5646.2009.00926.x) PubMed DOI

Barreto E, Lim MCW, Rojas D, Dávalos LM, Wüest RO, Machac A, Graham CH. 2023. Morphology and niche evolution influence hummingbird speciation rates. Figshare. (10.6084/m9.figshare.c.6533971) PubMed DOI PMC

Morphology and niche evolution influence hummingbird speciation rates