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      Phylogenetic test of speciation by host shift in leaf cone moths ( Caloptilia) feeding on maples ( Acer)

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          Abstract

          The traditional explanation for the exceptional diversity of herbivorous insects emphasizes host shift as the major driver of speciation. However, phylogenetic studies have often demonstrated widespread host plant conservatism by insect herbivores, calling into question the prevalence of speciation by host shift to distantly related plants. A limitation of previous phylogenetic studies is that host plants were defined at the family or genus level; thus, it was unclear whether host shifts predominate at a finer taxonomic scale. The lack of a statistical approach to test the hypothesis of host‐shift‐driven speciation also hindered studies at the species level. Here, we analyze the radiation of leaf cone moths ( Caloptilia) associated with maples ( Acer) using a newly developed, phylogeny‐based method that tests the role of host shift in speciation. This method has the advantage of not requiring complete taxon sampling from an entire radiation. Based on 254 host plant records for 14 Caloptilia species collected at 73 sites in Japan, we show that major dietary changes are more concentrated toward the root of the phylogeny, with host shift playing a minor role in recent speciation. We suggest that there may be other roles for host shift in promoting herbivorous insect diversification rather than facilitating speciation per se.

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          Stick insect genomes reveal natural selection's role in parallel speciation.

          Natural selection can drive the repeated evolution of reproductive isolation, but the genomic basis of parallel speciation remains poorly understood. We analyzed whole-genome divergence between replicate pairs of stick insect populations that are adapted to different host plants and undergoing parallel speciation. We found thousands of modest-sized genomic regions of accentuated divergence between populations, most of which are unique to individual population pairs. We also detected parallel genomic divergence across population pairs involving an excess of coding genes with specific molecular functions. Regions of parallel genomic divergence in nature exhibited exceptional allele frequency changes between hosts in a field transplant experiment. The results advance understanding of biological diversification by providing convergent observational and experimental evidence for selection's role in driving repeatable genomic divergence. Copyright © 2014, American Association for the Advancement of Science.
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            Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions.

            Diversification rate is one of the most important metrics in macroecological and macroevolutionary studies. Here I demonstrate that diversification analyses can be misleading when researchers assume that diversity increases unbounded through time, as is typical in molecular phylogenetic studies. If clade diversity is regulated by ecological factors, then species richness may be independent of clade age and it may not be possible to infer the rate at which diversity arose. This has substantial consequences for the interpretation of many studies that have contrasted rates of diversification among clades and regions. Often, it is possible to estimate the total diversification experienced by a clade but not diversification rate itself. I show that the evidence for ecological limits on diversity in higher taxa is widespread. Finally, I explore the implications of ecological limits for a variety of ecological and evolutionary questions that involve inferences about speciation and extinction rates from phylogenetic data.
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              Host-plant adaptation drives the parallel evolution of reproductive isolation.

              Parallel evolution of similar traits in independent populations that inhabit ecologically similar environments strongly implicates natural selection as the cause of evolution. Parallel speciation is a special form of parallel evolution where traits that determine reproductive isolation evolve repeatedly, in closely related populations, as by-products of adaptation to ecological conditions. The outcome of such parallel evolution is that ecologically divergent pairs of populations exhibit greater levels of reproductive isolation than ecologically similar pairs of populations of a similar or younger age. The parallel evolution of reproductive isolation provides strong evidence for natural selection in the process of speciation, but only one conclusive example from nature is known. Populations of the walking-stick insect Timema cristinae that use different host-plant species have diverged in body size and shape, host preference, behaviour and the relative frequency of two highly cryptic colour-pattern morphs. Here we report that divergent selection for host adaptation, and not genetic drift, has promoted the parallel evolution of sexual isolation in this species. Our findings represent a clear demonstration that host-plant adaptation can play a crucial and repeatable role in the early stages of speciation.
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                Author and article information

                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                21 June 2016
                July 2016
                : 6
                : 14 ( doiID: 10.1002/ece3.2016.6.issue-14 )
                : 4958-4970
                Affiliations
                [ 1 ] Center for Ecological ResearchKyoto University Hirano 2‐509‐3 Otsu Shiga 520‐2113Japan
                Author notes
                [*] [* ] Correspondence

                Ryosuke Nakadai, Center for Ecological Research, Kyoto University, Hirano 2‐509‐3, Otsu, Shiga 520‐2113, Japan.

                Tel: +81‐77‐549‐8018;

                Fax: +81‐77‐549‐8201;

                E‐mail: r.nakadai@ 123456ecology.kyoto-u.ac.jp

                Article
                ECE32266
                10.1002/ece3.2266
                4979720
                27547326
                9e7919f9-14f1-4ffa-bdb7-697651e08027
                © 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 12 May 2016
                : 26 May 2016
                : 27 May 2016
                Page count
                Pages: 13
                Funding
                Funded by: Japan Society for the Promotion of Science
                Award ID: 15H04421
                Award ID: 15J00601
                Award ID: 26650165
                Funded by: Joint Usage/Research Center, Field Science Center for Northern Biosphere, Hokkaido University
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece32266
                July 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:10.08.2016

                Evolutionary Biology
                diversification,herbivorous insect,host plant,host shift,speciation
                Evolutionary Biology
                diversification, herbivorous insect, host plant, host shift, speciation

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