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      Do major host shifts spark diversification in butterflies?

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          Abstract

          The Escape and Radiate Hypothesis posits that herbivorous insects and their host plants diversify through antagonistic coevolutionary adaptive radiation. For more than 50 years, it has inspired predictions about herbivorous insect macro‐evolution, but only recently have the resources begun to fall into place for rigorous testing of those predictions. Here, with comparative phylogenetic analyses of nymphalid butterflies, we test two of these predictions: that major host switches tend to increase species diversification and that such increases will be proportional to the scope of ecological opportunity afforded by a particular novel host association. We find that by and large the effect of major host‐use changes on butterfly diversity is the opposite of what was predicted; although it appears that the evolution of a few novel host associations can cause short‐term bursts of speciation, in general, major changes in host use tend to be linked to significant long‐term decreases in butterfly species richness.

          Abstract

          We test several key predictions of the Escape and Radiate Hypothesis using comparative phylogenetics in nymphalid butterflies. We find that although it appears that the evolution of a few novel host associations may have caused bursts of speciation, in general, major changes in host use tend to be linked to significant decreases in butterfly species richness.

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          Most cited references 36

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          Butterflies and Plants: A Study in Coevolution

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            Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades.

            Founder-event speciation, where a rare jump dispersal event founds a new genetically isolated lineage, has long been considered crucial by many historical biogeographers, but its importance is disputed within the vicariance school. Probabilistic modeling of geographic range evolution creates the potential to test different biogeographical models against data using standard statistical model choice procedures, as long as multiple models are available. I re-implement the Dispersal-Extinction-Cladogenesis (DEC) model of LAGRANGE in the R package BioGeoBEARS, and modify it to create a new model, DEC + J, which adds founder-event speciation, the importance of which is governed by a new free parameter, [Formula: see text]. The identifiability of DEC and DEC + J is tested on data sets simulated under a wide range of macroevolutionary models where geography evolves jointly with lineage birth/death events. The results confirm that DEC and DEC + J are identifiable even though these models ignore the fact that molecular phylogenies are missing many cladogenesis and extinction events. The simulations also indicate that DEC will have substantially increased errors in ancestral range estimation and parameter inference when the true model includes + J. DEC and DEC + J are compared on 13 empirical data sets drawn from studies of island clades. Likelihood-ratio tests indicate that all clades reject DEC, and AICc model weights show large to overwhelming support for DEC + J, for the first time verifying the importance of founder-event speciation in island clades via statistical model choice. Under DEC + J, ancestral nodes are usually estimated to have ranges occupying only one island, rather than the widespread ancestors often favored by DEC. These results indicate that the assumptions of historical biogeography models can have large impacts on inference and require testing and comparison with statistical methods. © The Author(s) 2014. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
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              Ecological opportunity and the origin of adaptive radiations.

              Ecological opportunity--through entry into a new environment, the origin of a key innovation or extinction of antagonists--is widely thought to link ecological population dynamics to evolutionary diversification. The population-level processes arising from ecological opportunity are well documented under the concept of ecological release. However, there is little consensus as to how these processes promote phenotypic diversification, rapid speciation and adaptive radiation. We propose that ecological opportunity could promote adaptive radiation by generating specific changes to the selective regimes acting on natural populations, both by relaxing effective stabilizing selection and by creating conditions that ultimately generate diversifying selection. We assess theoretical and empirical evidence for these effects of ecological opportunity and review emerging phylogenetic approaches that attempt to detect the signature of ecological opportunity across geological time. Finally, we evaluate the evidence for the evolutionary effects of ecological opportunity in the diversification of Caribbean Anolis lizards. Some of the processes that could link ecological opportunity to adaptive radiation are well documented, but others remain unsupported. We suggest that more study is required to characterize the form of natural selection acting on natural populations and to better describe the relationship between ecological opportunity and speciation rates.
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                Author and article information

                Contributors
                nbh0006@auburn.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                26 February 2020
                April 2020
                : 10
                : 8 ( doiID: 10.1002/ece3.v10.8 )
                : 3636-3646
                Affiliations
                [ 1 ] Department of Entomology and Plant Pathology Auburn University Auburn AL USA
                Author notes
                [* ] Correspondence

                Nate B. Hardy, Department of Entomology and Plant Pathology, Auburn University, Auburn, AL 36849, USA.

                Email: nbh0006@ 123456auburn.edu

                Article
                ECE36116
                10.1002/ece3.6116
                7160180
                © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                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.

                Page count
                Figures: 4, Tables: 1, Pages: 11, Words: 7969
                Product
                Funding
                Funded by: Alabama Agricultural Experiment Station , open-funder-registry 10.13039/100008745;
                Funded by: National Science Foundation , open-funder-registry 10.13039/100000001;
                Award ID: 1744552
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                April 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.0 mode:remove_FC converted:15.04.2020

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