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      Convergent evolution of toxin resistance in animals

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          ABSTRACT

          Convergence is the phenomenon whereby similar phenotypes evolve independently in different lineages. One example is resistance to toxins in animals. Toxins have evolved many times throughout the tree of life. They disrupt molecular and physiological pathways in target species, thereby incapacitating prey or deterring a predator. In response, molecular resistance has evolved in many species exposed to toxins to counteract their harmful effects. Here, we review current knowledge on the convergence of toxin resistance using examples from a wide range of toxin families. We explore the evolutionary processes and molecular adaptations driving toxin resistance. However, resistance adaptations may carry a fitness cost if they disrupt the normal physiology of the resistant animal. Therefore, there is a trade‐off between maintaining a functional molecular target and reducing toxin susceptibility. There are relatively few solutions that satisfy this trade‐off. As a result, we see a small set of molecular adaptations appearing repeatedly in diverse animal lineages, a phenomenon that is consistent with models of deterministic evolution. Convergence may also explain what has been called ‘autoresistance’. This is often thought to have evolved for self‐protection, but we argue instead that it may be a consequence of poisonous animals feeding on toxic prey. Toxin resistance provides a unique and compelling model system for studying the interplay between trophic interactions, selection pressures and the molecular mechanisms underlying evolutionary novelties.

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          Most cited references269

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          TimeTree: A Resource for Timelines, Timetrees, and Divergence Times.

          Evolutionary information on species divergence times is fundamental to studies of biodiversity, development, and disease. Molecular dating has enhanced our understanding of the temporal patterns of species divergences over the last five decades, and the number of studies is increasing quickly due to an exponential growth in the available collection of molecular sequences from diverse species and large number of genes. Our TimeTree resource is a public knowledge-base with the primary focus to make available all species divergence times derived using molecular sequence data to scientists, educators, and the general public in a consistent and accessible format. Here, we report a major expansion of the TimeTree resource, which more than triples the number of species (>97,000) and more than triples the number of studies assembled (>3,000). Furthermore, scientists can access not only the divergence time between two species or higher taxa, but also a timetree of a group of species and a timeline that traces a species' evolution through time. The new timetree and timeline visualizations are integrated with display of events on earth and environmental history over geological time, which will lead to broader and better understanding of the interplay of the change in the biosphere with the diversity of species on Earth. The next generation TimeTree resource is publicly available online at http://www.timetree.org.
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            Arms Races between and within Species

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              Complex cocktails: the evolutionary novelty of venoms.

              Venoms have evolved on numerous occasions throughout the animal kingdom. These 'biochemical weapon systems' typically function to facilitate, or protect the producing animal from, predation. Most venomous animals remain unstudied despite venoms providing model systems for investigating predator-prey interactions, molecular evolution, functional convergence, and novel targets for pharmaceutical discovery. Through advances in 'omic' technologies, venom composition data have recently become available for several venomous lineages, revealing considerable complexity in the processes responsible for generating the genetic and functional diversity observed in many venoms. Here, we review these recent advances and highlight the ecological and evolutionary novelty of venom systems. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                joryvthiel@gmail.com
                m.k.richardson@biology.leidenuniv.nl
                Journal
                Biol Rev Camb Philos Soc
                Biol Rev Camb Philos Soc
                10.1111/(ISSN)1469-185X
                BRV
                Biological Reviews of the Cambridge Philosophical Society
                Blackwell Publishing Ltd (Oxford, UK )
                1464-7931
                1469-185X
                17 May 2022
                October 2022
                : 97
                : 5 ( doiID: 10.1111/brv.v97.5 )
                : 1823-1843
                Affiliations
                [ 1 ] Institute of Biology Leiden Leiden University Sylviusweg 72, 2333 BE Leiden The Netherlands
                [ 2 ] Venom Evolution Lab, School of Biological Sciences University of Queensland St Lucia 4072 Australia
                [ 3 ] Centre for Snakebite Research & Interventions Liverpool School of Tropical Medicine Pembroke Place, Liverpool L3 5QA U.K.
                [ 4 ] Department of Biological Sciences National University of Singapore Singapore 117558 Singapore
                [ 5 ] Department of Pharmacology, Yong Loo Lin School of Medicine National University of Singapore Singapore 117600 Singapore
                [ 6 ] Department of Biochemistry, Medical College of Virginia Virginia Commonwealth University Richmond VA 23298 U.S.A.
                [ 7 ] School of Biological Sciences University of Northern Colorado Greeley CO 80639‐0017 U.S.A.
                [ 8 ] Naturalis Biodiversity Center Darwinweg 2, 2333 CR Leiden The Netherlands
                [ 9 ] Amsterdam Institute of Molecular and Life Sciences, Division of BioAnalytical Chemistry, Department of Chemistry and Pharmaceutical Sciences Vrije Universiteit Amsterdam De Boelelaan 1085, 1081HV Amsterdam The Netherlands
                [ 10 ] Molecular Ecology and Fisheries Genetics Laboratory, School of Natural Sciences Bangor University Bangor LL57 2UW U.K.
                Author notes
                [*] [* ] Authors for correspondence (Tel: +31 71 527 5215; E‐mail: joryvthiel@ 123456gmail.com ); (Tel: +31 71 527 5215; E‐mail: m.k.richardson@ 123456biology.leidenuniv.nl )

                Author information
                https://orcid.org/0000-0002-5187-7342
                https://orcid.org/0000-0003-1222-8101
                Article
                BRV12865
                10.1111/brv.12865
                9543476
                35580905
                ec69b44d-db08-4e13-8bae-41a4b6b1e5dc
                © 2022 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.

                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.

                History
                : 22 April 2022
                : 17 November 2021
                : 26 April 2022
                Page count
                Figures: 8, Tables: 0, Pages: 21, Words: 20582
                Funding
                Funded by: Academy Ecology Funds of Royal Netherlands Academy Of Arts And Sciences
                Award ID: 713/18015
                Funded by: Elise Mathilde Fonds of Leids Universiteits Fonds
                Award ID: 6113/21‐6‐16
                Funded by: Higher Education Commission, Islamabad, Pakistan
                Funded by: Ministry of Education, Singapore
                Award ID: MOE2017‐T2‐1‐045
                Funded by: University of Queensland International PhD scholarship fund
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                October 2022
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.0 mode:remove_FC converted:07.10.2022

                Ecology
                convergent evolution,toxin resistance,molecular adaptation,functional constraint,deterministic evolution,co‐evolutionary arms races

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