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      Adaptive divergence in shell morphology in an ongoing gastropod radiation from Lake Malawi

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          Abstract

          Background

          Ecological speciation is a prominent mechanism of diversification but in many evolutionary radiations, particularly in invertebrates, it remains unclear whether supposedly critical ecological traits drove or facilitated diversification. As a result, we lack accurate knowledge on the drivers of diversification for most evolutionary radiations along the tree of life. Freshwater mollusks present an enigmatic example: Putatively adaptive radiations are being described in various families, typically from long-lived lakes, whereas other taxa represent celebrated model systems in the study of ecophenotypic plasticity. Here we examine determinants of shell-shape variation in three nominal species of an ongoing ampullariid radiation in the Malawi Basin ( Lanistes nyassanus, L. solidus and Lanistes sp. ( ovum-like)) with a common garden experiment and semi-landmark morphometrics.

          Results

          We found significant differences in survival and fecundity among these species in contrasting habitats. Morphological differences observed in the wild persisted in our experiments for L. nyassanus versus L. solidus and L. sp. ( ovum-like), but differences between L. solidus and L. sp. ( ovum-like) disappeared and re-emerged in the F 1 and F 2 generations, respectively. These results indicate that plasticity occurred, but that it is not solely responsible for the observed differences. Our experiments provide the first unambiguous evidence for genetic divergence in shell morphology in an ongoing freshwater gastropod radiation in association with marked fitness differences among species under controlled habitat conditions.

          Conclusions

          Our results indicate that differences in shell morphology among Lanistes species occupying different habitats have an adaptive value. These results also facilitate an accurate reinterpretation of morphological variation in fossil Lanistes radiations, and thus macroevolutionary dynamics. Finally, our work testifies that the shells of freshwater gastropods may retain signatures of adaptation at low taxonomic levels, beyond representing an evolutionary novelty responsible for much of the diversity and disparity in mollusks altogether.

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          Most cited references48

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          Phenotypic plasticity's impacts on diversification and speciation.

          Phenotypic plasticity (the ability of a single genotype to produce multiple phenotypes in response to variation in the environment) is commonplace. Yet its evolutionary significance remains controversial, especially in regard to whether and how it impacts diversification and speciation. Here, we review recent theory on how plasticity promotes: (i) the origin of novel phenotypes, (ii) divergence among populations and species, (iii) the formation of new species and (iv) adaptive radiation. We also discuss the latest empirical support for each of these evolutionary pathways to diversification and identify potentially profitable areas for future research. Generally, phenotypic plasticity can play a largely underappreciated role in driving diversification and speciation. Copyright (c) 2010 Elsevier Ltd. All rights reserved.
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            Natural selection and the heritability of fitness components.

            The hypothesis that traits closely associated with fitness will generally possess lower heritabilities than traits more loosely connected with fitness is tested using 1120 narrow sense heritability estimates for wild, outbred animal populations, collected from the published record. Our results indicate that life history traits generally possess lower heritabilities than morphological traits, and that the means, medians, and cumulative frequency distributions of behavioural and physiological traits are intermediate between life history and morphological traits. These findings are consistent with popular interpretations of Fisher's (1930, 1958) Fundamental Theorem of Natural Selection, and Falconer (1960, 1981), but also indicate that high heritabilities are maintained within natural populations even for traits believed to be under strong selection. It is also found that the heritability of morphological traits is significantly lower for ectotherms than it is for endotherms which may in part be a result of the strong correlation between life history and body size for many ectotherms.
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              Evolutionary Strategies and Morphological Innovations: Cichlid Pharyngeal Jaws

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                Author and article information

                Contributors
                bert.van-bocxlaer@univ-lille.fr
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                9 January 2020
                9 January 2020
                2020
                : 20
                : 5
                Affiliations
                [1 ]ISNI 0000 0001 2242 6780, GRID grid.503422.2, CNRS, Univ. Lille, UMR 8198 – Evo-Eco-Paleo, ; F-59000 Lille, France
                [2 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Limnology Unit, Department of Biology, , Ghent University, ; 9000 Ghent, Belgium
                [3 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Geology, , Ghent University, ; 9000 Ghent, Belgium
                Author information
                https://orcid.org/0000-0003-2033-326X
                Article
                1570
                10.1186/s12862-019-1570-5
                6953155
                31918659
                a2b16b56-312f-44eb-a0dc-d1592fbff649
                © The Author(s). 2020

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 1 February 2019
                : 19 December 2019
                Funding
                Funded by: Agence Nationale de la Recherche
                Award ID: ANR-JCJC-EVOLINK
                Funded by: FundRef http://dx.doi.org/10.13039/501100003130, Fonds Wetenschappelijk Onderzoek;
                Award ID: 12N3915N
                Funded by: FundRef http://dx.doi.org/10.13039/501100008530, European Regional Development Fund;
                Award ID: FEDER-ERC-EVORAD
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2020

                Evolutionary Biology
                common garden experiment,geometric morphometrics,adaptive radiation,ampullariidae,phenotypic plasticity,differential fitness,local adaptation

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