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1AbstractPatterns of biological diversity across the tree of life are the result of millions of years of evolutionary history and are shaped by natural selection. A long-standing proposal is that most morphological diversity at a macroevolutionary scale (among species) arises along a microevolutionary “line of least resistance”. However, we frequently observe major shifts in phenotypes among lineages [1, 2, 3], suggesting that species or clades may also evolve away from the line of least resistance [4]. At the macroevolutionary scale, evolution along a common major axis has been termed elaboration whereas evolution away from that major axis is termed innovation [5]. The extent to which species and clades elaborate or innovate is poorly understood. Of particular importance is the potential contribution of reorientations of phenotypic trait space (innovation) among clades to contribute to the origins and maintenance of biodiversity across scales from the macro-to mega-evolutionary scale. Here we apply new multi-trait methods that model the nested covariance structure of traits to evaluate the magnitude and distribution of elaboration and innovation in the evolution of bird beaks. Our analyses show that elaboration dominates species-level phenotypic divergence, consistent with microevolutionary theory. However, innovation is surprisingly common at the clade level suggesting multiple routes to phenotypic innovation throughout avian evolutionary history. Our results highlight the importance of scale in our understanding of deep time evolution. While we find that elaboration dominates at macroevolutionary scales (i.e. species diverging within clades), the major axis of phenotypic change at megaevolutionary scales is an emergent property of innovation across clades. Taken together we suggest that innovation and elaboration are ubiquitous routes for phenotypic change but that their contribution to diversity is dependent on scale. The macroevolutionary axes of multivariate evolution are frequently reoriented throughout the history of life, opening up new avenues for evolution to explore.

Tobias, Joseph A., Sheard, Catherine, Pigot, Alex L., Devenish, Adam J. M., Yang, Jingyi, Sayol, Ferran, Neate‐Clegg, Montague H. C., Alioravainen, Nico, Weeks, Thomas L., Barber, Robert A., Walkden, Patrick A., MacGregor, Hannah E. A., Jones, Samuel E. I., Vincent, Claire, Phillips, Anna G., Marples, Nicola M., Montaño‐Centellas, Flavia A., Leandro‐Silva, Victor, Claramunt, Santiago, Darski, Bianca, Freeman, Benjamin G., Bregman, Tom P., Cooney, Christopher R., Hughes, Emma C., Capp, Elliot J. R., Varley, Zoë K., Friedman, Nicholas R., Korntheuer, Heiko, Corrales‐Vargas, Andrea, Trisos, Christopher H., Weeks, Brian C., Hanz, Dagmar M., Töpfer, Till, Bravo, Gustavo A., Remeš, Vladimír, Nowak, Larissa, Carneiro, Lincoln S., Moncada R., Amilkar J., Matysioková, Beata, Baldassarre, Daniel T., Martínez‐Salinas, Alejandra, Wolfe, Jared D., Chapman, Philip M., Daly, Benjamin G., Sorensen, Marjorie C., Neu, Alexander, Ford, Michael A., Mayhew, Rebekah J., Fabio Silveira, Luis, Kelly, David J., Annorbah, Nathaniel N. D., Pollock, Henry S., Grabowska‐Zhang, Ada M., McEntee, Jay P., Carlos T. Gonzalez, Juan, Meneses, Camila G., Muñoz, Marcia C., Powell, Luke L., Jamie, Gabriel A., Matthews, Thomas J., Johnson, Oscar, Brito, Guilherme R. R., Zyskowski, Kristof, Crates, Ross, Harvey, Michael G., Jurado Zevallos, Maura, Hosner, Peter A., Bradfer‐Lawrence, Tom, Maley, James M., Stiles, F. Gary, Lima, Hevana S., Provost, Kaiya L., Chibesa, Moses, Mashao, Mmatjie, Howard, Jeffrey T., Mlamba, Edson, Chua, Marcus A. H., Li, Bicheng, Gómez, M. Isabel, García, Natalia C., Päckert, Martin, Fuchs, Jérôme, Ali, Jarome R., Derryberry, Elizabeth P., Carlson, Monica L., Urriza, Rolly C., Brzeski, Kristin E., Prawiradilaga, Dewi M., Rayner, Matt J., Miller, Eliot T., Bowie, Rauri C. K., Lafontaine, René‐Marie, Scofield, R. Paul, Lou, Yingqiang, Somarathna, Lankani, Lepage, Denis, Illif, Marshall, Neuschulz, Eike Lena, Templin, Mathias, Dehling, D. Matthias, Cooper, Jacob C., Pauwels, Olivier S. G., Analuddin, Kangkuso, Fjeldså, Jon, Seddon, Nathalie, Sweet, Paul R., DeClerck, Fabrice A. J., Naka, Luciano N., Brawn, Jeffrey D., Aleixo, Alexandre, Böhning‐Gaese, Katrin, Rahbek, Carsten, Fritz, Susanne A., Thomas, Gavin H., Schleuning, Matthias (2022): AVONET: morphological, ecological and geographical data for all birds. Ecology Letters 25 (3): 581-597, DOI: 10.1111/ele.13898, URL: http://dx.doi.org/10.1111/ele.13898

Trapliners are pollinators that visit widely dispersed flowers along circuitous foraging routes. The evolution of traplining in hummingbirds is thought to entail morphological specialization through the reciprocal coevolution of longer bills with the long-tubed flowers of widely dispersed plant species. Specialization, such as that exhibited by traplining hummingbirds, is often viewed as both irreversible and an evolutionary dead end. We tested these predictions in a macroevolutionary framework. Specifically, we assessed the relationship between beak morphology and foraging and tested whether transitions to traplining are irreversible and lead to lower rates of diversification as predicted by the hypothesis that specialization is an evolutionary dead end. We find that there have been multiple independent transitions to traplining across the hummingbird phylogeny, but reversals have been rare or incomplete at best. Multiple independent lineages of trapliners have become morphologically specialized, convergently evolving relatively large bills for their body size. Traplining is not an evolutionary dead end however, since trapliners continue to give rise to new traplining species at a rate comparable to non-trapliners.

Biodiversity is facing a global extinction crisis that will reduce ecological trait diversity, evolutionary history, and ultimately ecosystem functioning and services.