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      A fly in a tube: Macroevolutionary expectations for integrated phenotypes

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          Abstract

          Phenotypic integration and modularity are ubiquitous features of complex organisms, describing the magnitude and pattern of relationships among biological traits. A key prediction is that these relationships, reflecting genetic, developmental, and functional interactions, shape evolutionary processes by governing evolvability and constraint. Over the last 60 years, a rich literature of research has quantified patterns of integration and modularity across a variety of clades and systems. Only recently has it become possible to contextualize these findings in a phylogenetic framework to understand how trait integration interacts with evolutionary tempo and mode. Here, we review the state of macroevolutionary studies of integration and modularity, synthesizing empirical and theoretical work into a conceptual framework for predicting the effects of integration on evolutionary rate and disparity: a fly in a tube. While magnitude of integration is expected to influence the potential for phenotypic variation to be produced and maintained, thus defining the shape and size of a tube in morphospace, evolutionary rate, or the speed at which a fly moves around the tube, is not necessarily controlled by trait interactions. Finally, we demonstrate this reduced disparity relative to the Brownian expectation for a given rate of evolution with an empirical example: the avian cranium.

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          Punctuated equilibria: the tempo and mode of evolution reconsidered

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            Flowering Plants

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              PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY.

              The problem of complex adaptations is studied in two largely disconnected research traditions: evolutionary biology and evolutionary computer science. This paper summarizes the results from both areas and compares their implications. In evolutionary computer science it was found that the Darwinian process of mutation, recombination and selection is not universally effective in improving complex systems like computer programs or chip designs. For adaptation to occur, these systems must possess "evolvability," i.e., the ability of random variations to sometimes produce improvement. It was found that evolvability critically depends on the way genetic variation maps onto phenotypic variation, an issue known as the representation problem. The genotype-phenotype map determines the variability of characters, which is the propensity to vary. Variability needs to be distinguished from variations, which are the actually realized differences between individuals. The genotype-phenotype map is the common theme underlying such varied biological phenomena as genetic canalization, developmental constraints, biological versatility, developmental dissociability, and morphological integration. For evolutionary biology the representation problem has important implications: how is it that extant species acquired a genotype-phenotype map which allows improvement by mutation and selection? Is the genotype-phenotype map able to change in evolution? What are the selective forces, if any, that shape the genotype-phenotype map? We propose that the genotype-phenotype map can evolve by two main routes: epistatic mutations, or the creation of new genes. A common result for organismic design is modularity. By modularity we mean a genotype-phenotype map in which there are few pleiotropic effects among characters serving different functions, with pleiotropic effects falling mainly among characters that are part of a single functional complex. Such a design is expected to improve evolvability by limiting the interference between the adaptation of different functions. Several population genetic models are reviewed that are intended to explain the evolutionary origin of a modular design. While our current knowledge is insufficient to assess the plausibility of these models, they form the beginning of a framework for understanding the evolution of the genotype-phenotype map.
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                Author and article information

                Contributors
                a.goswami@nhm.ac.uk
                Journal
                Evolution
                Evolution
                10.1111/(ISSN)1558-5646
                EVO
                Evolution; International Journal of Organic Evolution
                John Wiley and Sons Inc. (Hoboken )
                0014-3820
                1558-5646
                08 October 2018
                December 2018
                : 72
                : 12 ( doiID: 10.1111/evo.2018.72.issue-12 )
                : 2580-2594
                Affiliations
                [ 1 ] Department of Life Sciences The Natural History Museum London SW7 5DB United Kingdom
                [ 2 ] Department of Genetics, Evolution, and Environment University College London London WC1E 6BT United Kingdom
                Article
                EVO13608
                10.1111/evo.13608
                6585935
                30246245
                19767765-45d0-4eac-8d91-cb5f2ed89823
                © 2018 The Author(s). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                Page count
                Figures: 6, Tables: 1, Pages: 15, Words: 10749
                Product
                Funding
                Funded by: ERC
                Award ID: STG‐2014‐637171
                Funded by: Leverhulme Trust
                Award ID: RPG 2013‐124
                Funded by: SYNTHESIS
                Award ID: FR‐TAF‐5635
                Categories
                Perspective
                Perspective
                Custom metadata
                2.0
                evo13608
                December 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.4 mode:remove_FC converted:20.06.2019

                Evolutionary Biology
                constraints,disparity,evolutionary rates,macroevolution,modularity,phenotypic integration

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