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      Variation of chemical compounds in wild Heliconiini reveals ecological factors involved in the evolution of chemical defenses in mimetic butterflies

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          Abstract

          Evolutionary convergence of color pattern in mimetic species is tightly linked with the evolution of chemical defenses. Yet, the evolutionary forces involved in natural variations of chemical defenses in aposematic species are still understudied. Herein, we focus on the evolution of chemical defenses in the butterfly tribe Heliconiini. These neotropical butterflies contain large concentrations of cyanogenic glucosides, cyanide‐releasing compounds acting as predator deterrent. These compounds are either de novo synthesized or sequestered from their Passiflora host plant, so that their concentrations may depend on host plant specialization and host plant availability. We sampled 375 wild Heliconiini butterflies across Central and South America, covering 43% species of this clade, and quantify individual variations in the different CGs using liquid chromatography coupled with tandem mass spectrometry. We detected new compounds and important variations in chemical defenses both within and among species. Based on the most recent and well‐studied phylogeny of Heliconiini, we show that ecological factors such as mimetic interactions and host plant specialization have a significant association with chemical profiles, but these effects are largely explained by phylogenetic relationships. Our results therefore suggest that shared ancestries largely contribute to chemical defense variation, pointing out at the interaction between historical and ecological factors in the evolution of Müllerian mimicry.

          Abstract

          Within Heliconiini butterflies, we show that ecological factors such as mimetic interactions and host plant specialization have a significant effect on chemical profiles, but these effects are largely explained by phylogenetic relationships. Our results suggest that shared ancestries largely contribute to chemical defence variation, pointing out at the interaction between historical and ecological factors in the evolution of Müllerian mimicry.

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          Most cited references57

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          A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data.

          Phylogenetic signal is the tendency for closely related species to display similar trait values due to their common ancestry. Several methods have been developed for quantifying phylogenetic signal in univariate traits and for sets of traits treated simultaneously, and the statistical properties of these approaches have been extensively studied. However, methods for assessing phylogenetic signal in high-dimensional multivariate traits like shape are less well developed, and their statistical performance is not well characterized. In this article, I describe a generalization of the K statistic of Blomberg et al. that is useful for quantifying and evaluating phylogenetic signal in highly dimensional multivariate data. The method (K(mult)) is found from the equivalency between statistical methods based on covariance matrices and those based on distance matrices. Using computer simulations based on Brownian motion, I demonstrate that the expected value of K(mult) remains at 1.0 as trait variation among species is increased or decreased, and as the number of trait dimensions is increased. By contrast, estimates of phylogenetic signal found with a squared-change parsimony procedure for multivariate data change with increasing trait variation among species and with increasing numbers of trait dimensions, confounding biological interpretations. I also evaluate the statistical performance of hypothesis testing procedures based on K(mult) and find that the method displays appropriate Type I error and high statistical power for detecting phylogenetic signal in high-dimensional data. Statistical properties of K(mult) were consistent for simulations using bifurcating and random phylogenies, for simulations using different numbers of species, for simulations that varied the number of trait dimensions, and for different underlying models of trait covariance structure. Overall these findings demonstrate that K(mult) provides a useful means of evaluating phylogenetic signal in high-dimensional multivariate traits. Finally, I illustrate the utility of the new approach by evaluating the strength of phylogenetic signal for head shape in a lineage of Plethodon salamanders.
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            Sequestration of defensive substances from plants by Lepidoptera.

            A number of aposematic butterfly and diurnal moth species sequester unpalatable or toxic substances from their host plants rather than manufacturing their own defensive substances. Despite a great diversity in their life histories, there are some general features in the selective utilization of plant secondary metabolites to achieve effective protection from predators. This review illustrates the biochemical, physiological, and ecological characteristics of phytochemical-based defense systems that can shed light on the evolution of the widely developed sequestering lifestyles among the Lepidoptera.
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              Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach.

              Understanding how and why certain clades diversify greatly in morphology whereas others do not remains a major theme in evolutionary biology. Projecting families of phylogenies into multivariate morphospaces can distinguish two scenarios potentially leading to unequal morphological diversification: unequal magnitude of change per phylogenetic branch, and unequal efficiency in morphological innovation. This approach is demonstrated using a case study of skulls in sister clades within the South American fish superfamily Anostomoidea. Unequal morphological diversification in this system resulted not from the morphologically diverse clade changing more on each phylogenetic branch, but from that clade distributing an equal amount of change more widely through morphospace and innovating continually. Although substantial morphological evolution occurred throughout the less diverse clade's history, most of that clade's expansion in morphospace occurred in the most basal branches, and more derived portions of that radiation oscillated within previously explored limits. Because simulations revealed that there is a maximum 2.7% probability of generating two clades that differ so greatly in the density of lineages within morphospace under a null Brownian model, the observed difference in pattern likely reflects a difference in the underlying evolutionary process. Clade-specific factors that may have promoted or arrested morphological diversification are discussed.
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                Author and article information

                Contributors
                ombelinesculfort@hotmail.fr
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                13 February 2020
                March 2020
                : 10
                : 5 ( doiID: 10.1002/ece3.v10.5 )
                : 2677-2694
                Affiliations
                [ 1 ] Institut de Systématique, Evolution, Biodiversité (ISYEB) Muséum National d'Histoire Naturelle CNRS Sorbonne‐Université EPHE Université des Antilles Paris France
                [ 2 ] Unité Molécules de Communication et Adaptations des Micro‐organismes (MCAM) Muséum National d'Histoire Naturelle CNRS Paris France
                [ 3 ] Department of Zoology Cambridge University Cambridge UK
                [ 4 ] Smithsonian Tropical Research Institute Panamá Panamá
                [ 5 ] Department of Plant and Environmental Sciences University of Copenhagen Frederiksberg Denmark
                [ 6 ] Laboratoire de Synthèse Organique Ecole Polytechnique CNRS ENSTA Institut Polytechnique de Paris Palaiseau Cedex France
                Author notes
                [*] [* ] Correspondence

                Ombeline Sculfort, Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne‐Université, EPHE, Université des Antilles, 45 rue Buffon, 75005 Paris, France.

                Email: ombelinesculfort@ 123456hotmail.fr

                Author information
                https://orcid.org/0000-0002-1583-824X
                https://orcid.org/0000-0002-4731-3835
                Article
                ECE36044
                10.1002/ece3.6044
                7069300
                32185010
                463d78d4-0f41-4cfc-a19a-3eb366089cd7
                © 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.

                History
                : 29 November 2019
                : 06 January 2020
                : 07 January 2020
                Page count
                Figures: 6, Tables: 4, Pages: 18, Words: 12785
                Funding
                Funded by: European Research Council , open-funder-registry 10.13039/501100000781;
                Award ID: 339873
                Funded by: Marie Curie Actions
                Funded by: Agence Nationale de la Recherche , open-funder-registry 10.13039/501100001665;
                Award ID: ANR‐10‐LABX‐0003‐BCDiv
                Award ID: ANR‐11‐IDEX‐0004‐02
                Categories
                Review
                Reviews
                Custom metadata
                2.0
                March 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.7 mode:remove_FC converted:13.03.2020

                Evolutionary Biology
                aposematism,cyanogenic glucosides,heliconius,lc‐ms/ms,müllerian mimicry,phylogenetic signal

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