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      Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians

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          Abstract

          The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.

          Abstract

          What selective pressures alter the tradeoff between offspring size and number? A phylogenetic comparative approach shows that amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviours and adaptations vary in their effects on the tradeoff.

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          Inferring the historical patterns of biological evolution.

          M. Pagel (1999)
          Phylogenetic trees describe the pattern of descent amongst a group of species. With the rapid accumulation of DNA sequence data, more and more phylogenies are being constructed based upon sequence comparisons. The combination of these phylogenies with powerful new statistical approaches for the analysis of biological evolution is challenging widely held beliefs about the history and evolution of life on Earth.
            Bookmark
            • Record: found
            • Abstract: not found
            • Article: not found

            AVIAN LIFE HISTORY VARIATION AND CONTRIBUTION OF DEMOGRAPHIC TRAITS TO THE POPULATION GROWTH RATE

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              Is Open Access

              Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees

              (2014)
              A number of methods have been developed to infer differential rates of species diversification through time and among clades using time-calibrated phylogenetic trees. However, we lack a general framework that can delineate and quantify heterogeneous mixtures of dynamic processes within single phylogenies. I developed a method that can identify arbitrary numbers of time-varying diversification processes on phylogenies without specifying their locations in advance. The method uses reversible-jump Markov Chain Monte Carlo to move between model subspaces that vary in the number of distinct diversification regimes. The model assumes that changes in evolutionary regimes occur across the branches of phylogenetic trees under a compound Poisson process and explicitly accounts for rate variation through time and among lineages. Using simulated datasets, I demonstrate that the method can be used to quantify complex mixtures of time-dependent, diversity-dependent, and constant-rate diversification processes. I compared the performance of the method to the MEDUSA model of rate variation among lineages. As an empirical example, I analyzed the history of speciation and extinction during the radiation of modern whales. The method described here will greatly facilitate the exploration of macroevolutionary dynamics across large phylogenetic trees, which may have been shaped by heterogeneous mixtures of distinct evolutionary processes.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: ResourcesRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                4 January 2022
                January 2022
                4 January 2022
                : 20
                : 1
                : e3001495
                Affiliations
                [1 ] Department of Biological and Marine Sciences, University of Hull, Hull, United Kingdom
                [2 ] Energy and Environment Institute, University of Hull, Hull, United Kingdom
                [3 ] School of Biological Sciences, University of Reading, Reading, United Kingdom
                [4 ] School of Biological Sciences, Queen’s University Belfast, Belfast, United Kingdom
                The Australian National University, AUSTRALIA
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-7596-9623
                https://orcid.org/0000-0001-8065-2436
                Article
                PBIOLOGY-D-21-01616
                10.1371/journal.pbio.3001495
                8726499
                34982764
                33d98380-7500-4118-b013-d223a7e51f69
                © 2022 Furness et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 18 June 2021
                : 26 November 2021
                Page count
                Figures: 3, Tables: 1, Pages: 20
                Funding
                Funded by: university of hull
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000873, queen's university belfast;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000275, leverhulme trust;
                Award ID: RPG-2017-017
                Award Recipient :
                We thank the University of Hull and Queen’s University Belfast for supporting this project with funding to IC, and Leverhulme Trust (Research Project Grant RPG-2017-017 to CV) for funding this research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Leverhulme Trust: https://www.leverhulme.ac.uk.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Eggs
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Clutches
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Evolutionary Rate
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Tadpoles
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amphibians
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Amphibians
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Eggs
                Bird Eggs
                Biology and Life Sciences
                Developmental Biology
                Evolutionary Developmental Biology
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Developmental Biology
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. The dataset compiled and analysed for this manuscript has been uploaded as S1 Data. The sources for the data are available in S1 Data and list in S3 Data. The phylogeny pruned from Pyron (2014) and used for the analysis is uploaded as S2 Data.

                Life sciences
                Life sciences

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