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      Investigating the evolution and development of biological complexity under the framework of epigenetics

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          Abstract

          Biological complexity is a key component of evolvability, yet its study has been hampered by a focus on evolutionary trends of complexification and inconsistent definitions. Here, we demonstrate the utility of bringing complexity into the framework of epigenetics to better investigate its utility as a concept in evolutionary biology. We first analyze the existing metrics of complexity and explore the link between complexity and adaptation. Although recently developed metrics allow for a unified framework, they omit developmental mechanisms. We argue that a better approach to the empirical study of complexity and its evolution includes developmental mechanisms. We then consider epigenetic mechanisms and their role in shaping developmental and evolutionary trajectories, as well as the development and organization of complexity. We argue that epigenetics itself could have emerged from complexity because of a need to self‐regulate. Finally, we explore hybridization complexes and hybrid organisms as potential models for studying the association between epigenetics and complexity. Our goal is not to explain trends in biological complexity but to help develop and elucidate novel questions in the investigation of biological complexity and its evolution.

          Abstract

          Biological complexity is the result of the hierarchical organisation of nested levels of cells, tissues and higher order part types interacting together.

          RESEARCH HIGHLIGHTS

          This manuscript argues that biological complexity is better understood under the framework of epigenetics and that the epigenetic interactions emerge from the self‐regulation of complex systems. Hybrids are offered as models to study these properties.

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          Most cited references125

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          Hybridization and speciation.

          Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. © 2013 The Authors. Journal of Evolutionary Biology © 2013 European Society For Evolutionary Biology.
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            Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation.

            Adaptation to a sudden extreme change in environment, beyond the usual range of background environmental fluctuations, is analysed using a quantitative genetic model of phenotypic plasticity. Generations are discrete, with time lag tau between a critical period for environmental influence on individual development and natural selection on adult phenotypes. The optimum phenotype, and genotypic norms of reaction, are linear functions of the environment. Reaction norm elevation and slope (plasticity) vary among genotypes. Initially, in the average background environment, the character is canalized with minimum genetic and phenotypic variance, and no correlation between reaction norm elevation and slope. The optimal plasticity is proportional to the predictability of environmental fluctuations over time lag tau. During the first generation in the new environment the mean fitness suddenly drops and the mean phenotype jumps towards the new optimum phenotype by plasticity. Subsequent adaptation occurs in two phases. Rapid evolution of increased plasticity allows the mean phenotype to closely approach the new optimum. The new phenotype then undergoes slow genetic assimilation, with reduction in plasticity compensated by genetic evolution of reaction norm elevation in the original environment.
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              Phenotypic plasticity and evolution by genetic assimilation.

              In addition to considerable debate in the recent evolutionary literature about the limits of the Modern Synthesis of the 1930s and 1940s, there has also been theoretical and empirical interest in a variety of new and not so new concepts such as phenotypic plasticity, genetic assimilation and phenotypic accommodation. Here we consider examples of the arguments and counter-arguments that have shaped this discussion. We suggest that much of the controversy hinges on several misunderstandings, including unwarranted fears of a general attempt at overthrowing the Modern Synthesis paradigm, and some fundamental conceptual confusion about the proper roles of phenotypic plasticity and natural selection within evolutionary theory.
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                Author and article information

                Contributors
                Kevin.duclos@ucalgary.ca
                Journal
                Evol Dev
                Evol. Dev
                10.1111/(ISSN)1525-142X
                EDE
                Evolution & Development
                John Wiley and Sons Inc. (Hoboken )
                1520-541X
                1525-142X
                03 July 2019
                September 2019
                : 21
                : 5 ( doiID: 10.1111/ede.v21.5 )
                : 276-293
                Affiliations
                [ 1 ] Department of Cell Biology and Anatomy The University of Calgary Calgary Alberta Canada
                [ 2 ] Department of Community Health Sciences The University of Calgary Calgary Alberta Canada
                Author notes
                [*] [* ] Correspondence Kevin Duclos, Department of Cell Biology and Anatomy, The University of Calgary, Calgary, Alberta, Canada. Email: Kevin.duclos@ 123456ucalgary.ca

                Author information
                http://orcid.org/0000-0003-3694-1171
                Article
                EDE12301
                10.1111/ede.12301
                6852014
                31268245
                b305c388-ee9f-4b10-9e73-12557a5b0cf6
                © 2019 The Authors. Evolution & Development Published by Wiley Periodicals, Inc.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Figures: 3, Tables: 0, Pages: 18, Words: 12803
                Categories
                Perspective
                Perspective
                Custom metadata
                2.0
                September 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.1 mode:remove_FC converted:13.11.2019

                Developmental biology
                biological complexity,development,epigenetics,evolution,hybridization
                Developmental biology
                biological complexity, development, epigenetics, evolution, hybridization

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