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      Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait

      research-article
      1 , 2 , 1 , 3 , 1 , 3 ,
      EvoDevo
      BioMed Central

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          Abstract

          Background

          Hox proteins specify segment identity during embryogenesis and have typical associated expression patterns. Changes in embryonic expression and activity of Hox genes were crucial in the evolution of animal body plans, but their role in the post-embryonic development of lineage-specific traits remains largely unexplored. Here, we focus on the insect Hox genes Ultrabithorax ( Ubx) and Antennapedia ( Antp), and implicate the latter in the formation and diversification of novel, butterfly-specific wing patterns.

          Results

          First, we describe a conserved pattern of Ubx expression and a novel pattern of Antp expression in wing discs of Bicyclus anynana butterflies. The discrete, reiterated domains of Antp contrast with the typical expression of Hox genes in single continuous regions in arthropod embryos. Second, we show that this pattern is associated with the establishment of the organizing centres of eyespots. Antp upregulation is the earliest event in organizer development described to date, and in contrast to all genes implicated in eyespot formation, is exclusive to those centres. Third, our comparative analysis of gene expression across nymphalids reveals unexpected differences in organizer determination.

          Conclusions

          We show that the Antp's recruitment for the formation of novel traits in butterfly wing discs involved the evolution of new expression domains, and is restricted to a particular lineage. This study contributes novel insights into the evolution of Antp expression, as well as into the genetic mechanisms underlying morphological diversification. Our results also underscore how a wider representation of morphological and phylogenetic diversity is essential in evolutionary developmental biology.

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          Most cited references54

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          Evo-devo: extending the evolutionary synthesis.

          Evolutionary developmental biology (evo-devo) explores the mechanistic relationships between the processes of individual development and phenotypic change during evolution. Although evo-devo is widely acknowledged to be revolutionizing our understanding of how the development of organisms has evolved, its substantial implications for the theoretical basis of evolution are often overlooked. This essay identifies major theoretical themes of current evo-devo research and highlights how its results take evolutionary theory beyond the boundaries of the Modern Synthesis.
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            Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary.

            The butterfly family Nymphalidae contains some of the most important non-drosophilid insect model systems for evolutionary and ecological studies, yet the evolutionary history of the group has remained shrouded in mystery. We have inferred a robust phylogenetic hypothesis based on sequences of 10 genes and 235 morphological characters for exemplars of 400 of the 540 valid nymphalid genera representing all major lineages of the family. By dating the branching events, we infer that Nymphalidae originated in the Cretaceous at 90 Ma, but that the ancestors of 10-12 lineages survived the end-Cretaceous catastrophe in the Neotropical and Oriental regions. Patterns of diversification suggest extinction of lineages at the Cretaceous/Tertiary boundary (65 Ma) and subsequent elevated speciation rates in the Tertiary.
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              • Record: found
              • Abstract: found
              • Article: not found

              Development, plasticity and evolution of butterfly eyespot patterns.

              The developmental and genetic bases for the formation, plasticity and diversity of eyespot patterns in butterflies are examined. Eyespot pattern mutants, regulatory gene expression, and transplants of the eyespot developmental organizer demonstrate that eyespot position, number, size and colour are determined progressively in a developmental pathway largely uncoupled from those regulating other wing-pattern elements and body structures. Species comparisons and selection experiments suggest that the evolution of eyespot patterns can occur rapidly through modulation of different stages of this pathway, and requires only single, or very few, changes in regulatory genes.
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                Author and article information

                Journal
                EvoDevo
                EvoDevo
                BioMed Central
                2041-9139
                2011
                19 April 2011
                : 2
                : 9
                Affiliations
                [1 ]Institute of Biology, Leiden University, Sylviusweg 72, 2333 BE Leiden, The Netherlands
                [2 ]Current Address: Department of Genetics and Evolution, University of Geneva, 1211 Geneva 4, Switzerland
                [3 ]Instituto Gulbenkian de Ciência, Rua da Quinta Grande 6, P-2780-156 Oeiras, Portugal
                Article
                2041-9139-2-9
                10.1186/2041-9139-2-9
                3108338
                21504568
                b17095f6-a55f-47e1-8628-142fdb9f6ec0
                Copyright ©2011 Saenko et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 24 January 2011
                : 19 April 2011
                Categories
                Research

                Developmental biology
                Developmental biology

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