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      Parental provisioning drives brain size in birds

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          Significance

          The young of large-brained species, if left to grow their own brain, would face a seemingly insurmountable energetic constraint, because brain tissue is energetically costly but adequate cognitive benefits arise only after a delay. We therefore hypothesize that protracted parental provisioning was a precondition for the evolution of large brains. Comparative analyses of 1,176 bird species confirmed that parental provisioning strongly predicts variation in relative brain size, suggesting that these two traits coevolved. These results provide an explanation for the well-known but so far unexplained difference in relative brain size between altricial and precocial birds. They also cast doubt on the explanatory value of previously considered social or technological cognitive abilities, suggesting we rethink our approach to cognitive evolution.

          Abstract

          Large brains support numerous cognitive adaptations and therefore may appear to be highly beneficial. Nonetheless, the high energetic costs of brain tissue may have prevented the evolution of large brains in many species. This problem may also have a developmental dimension: juveniles, with their immature and therefore poorly performing brains, would face a major energetic hurdle if they were to pay for the construction of their own brain, especially in larger-brained species. Here, we explore the possible role of parental provisioning for the development and evolution of adult brain size in birds. A comparative analysis of 1,176 bird species shows that various measures of parental provisioning (precocial vs. altricial state at hatching, relative egg mass, time spent provisioning the young) strongly predict relative brain size across species. The parental provisioning hypothesis also provides an explanation for the well-documented but so far unexplained pattern that altricial birds have larger brains than precocial ones. We therefore conclude that the evolution of parental provisioning allowed species to overcome the seemingly insurmountable energetic constraint on growing large brains, which in turn enabled bird species to increase survival and population stability. Because including adult eco- and socio-cognitive predictors only marginally improved the explanatory value of our models, these findings also suggest that the traditionally assessed cognitive abilities largely support successful parental provisioning. Our results therefore indicate that the cognitive adaptations underlying successful parental provisioning also provide the behavioral flexibility facilitating reproductive success and survival.

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          Most cited references82

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          MCMC Methods for Multi-Response Generalized Linear Mixed Models: TheMCMCglmmRPackage

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            The global diversity of birds in space and time.

            Current global patterns of biodiversity result from processes that operate over both space and time and thus require an integrated macroecological and macroevolutionary perspective. Molecular time trees have advanced our understanding of the tempo and mode of diversification and have identified remarkable adaptive radiations across the tree of life. However, incomplete joint phylogenetic and geographic sampling has limited broad-scale inference. Thus, the relative prevalence of rapid radiations and the importance of their geographic settings in shaping global biodiversity patterns remain unclear. Here we present, analyse and map the first complete dated phylogeny of all 9,993 extant species of birds, a widely studied group showing many unique adaptations. We find that birds have undergone a strong increase in diversification rate from about 50 million years ago to the near present. This acceleration is due to a number of significant rate increases, both within songbirds and within other young and mostly temperate radiations including the waterfowl, gulls and woodpeckers. Importantly, species characterized with very high past diversification rates are interspersed throughout the avian tree and across geographic space. Geographically, the major differences in diversification rates are hemispheric rather than latitudinal, with bird assemblages in Asia, North America and southern South America containing a disproportionate number of species from recent rapid radiations. The contribution of rapidly radiating lineages to both temporal diversification dynamics and spatial distributions of species diversity illustrates the benefits of an inclusive geographical and taxonomical perspective. Overall, whereas constituent clades may exhibit slowdowns, the adaptive zone into which modern birds have diversified since the Cretaceous may still offer opportunities for diversification.
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              EltonTraits 1.0: Species-level foraging attributes of the world's birds and mammals

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                Author and article information

                Contributors
                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                6 January 2023
                10 January 2023
                6 July 2023
                : 120
                : 2
                : e2121467120
                Affiliations
                [1] aDepartment of Biology, University of Konstanz , 78457 Konstanz, Germany
                [2] bCenter for the Advanced Study of Collective Behaviour, University of Konstanz , 78457 Konstanz, Germany
                [3] cDepartment of Collective Behavior, Max Planck Institute of Animal Behavior , 78457 Konstanz, Germany
                [4] dDepartment of Anthropology, University of Zurich , 8057 Zurich, Switzerland
                [5] eEvolution & Ecology Research Centre, School of Biological, Environmental & Earth Sciences, University of New South Wales , Sydney, NSW 2052, Australia
                [6] fInstitute of Environmental Sciences, Jagiellonian University , 30-387 Krakow, Poland
                [7] gCentre for Interdisciplinary Study of Language Evolution, University of Zurich , 8050 Zürich, Switzerland
                [8] hComparative Socioecology Group, Max Planck Institute for Animal Behavior , 78467 Konstanz, Germany
                Author notes
                1To whom correspondence may be addressed. Email: michael.griesser@ 123456uni-konstanz.de .

                Edited by Scott Edwards, Harvard University, Cambridge, MA; received December 22, 2021; accepted November 26, 2022

                Author information
                https://orcid.org/0000-0002-2220-2637
                Article
                202121467
                10.1073/pnas.2121467120
                9926254
                36608292
                a130dac1-a5a9-4cfe-af82-70ef9c601743
                Copyright © 2023 the Author(s). Published by PNAS.

                This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                : 22 December 2021
                : 26 November 2022
                Page count
                Pages: 10, Words: 5560
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG), FundRef 501100001659;
                Award ID: GR 4650/2-1
                Award Recipient : Michael Griesser
                Funded by: Narodowe Centrum Nauki (NCN), FundRef 501100004281;
                Award ID: UMO-2015/18/E/NZ8/00505
                Award Recipient : Szymon M Drobniak
                Categories
                dataset, Dataset
                research-article, Research Article
                evolution, Evolution
                418
                Biological Sciences
                Evolution

                precocial and altricial birds,cognitive evolution,expensive brain hypothesis,comparative study,brain development

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