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      Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals

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          Abstract

          Background

          Here we provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs. This unique group, which encapsulates diverse ecological modes, such as terrestrial, subterranean, and aquatic lifestyles, is used to examine the evolutionary lability of cranial osteogenesis and to investigate the modularity of development.

          Results

          An acceleration of developmental timing of the vomeronasal complex has occurred in the common ancestor of moles. However, ossification of the nasal bone has shifted late in the more terrestrial shrew mole. Among the lipotyphlans, sequence heterochrony shows no significant association with modules derived from developmental origins (that is, neural crest cells vs. mesoderm derived parts) or with those derived from ossification modes (that is, dermal vs. endochondral ossification).

          Conclusions

          The drastic acceleration of vomeronasal development in moles is most likely coupled with the increased importance of the rostrum for digging and its use as a specialized tactile surface, both fossorial adaptations. The late development of the nasal in shrew moles, a condition also displayed by hedgehogs and shrews, is suggested to be the result of an ecological reversal to terrestrial lifestyle and reduced functional importance of the rostrum. As an overall pattern in lipotyphlans, our results reject the hypothesis that ossification sequence heterochrony occurs in modular fashion when considering the developmental patterns of the skull. We suggest that shifts in the cranial ossification sequence are not evolutionarily constrained by developmental origins or mode of ossification.

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          Most cited references57

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          Is evolvability evolvable?

          In recent years, biologists have increasingly been asking whether the ability to evolve--the evolvability--of biological systems, itself evolves, and whether this phenomenon is the result of natural selection or a by-product of other evolutionary processes. The concept of evolvability, and the increasing theoretical and empirical literature that refers to it, may constitute one of several pillars on which an extended evolutionary synthesis will take shape during the next few years, although much work remains to be done on how evolvability comes about.
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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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              A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys.

              Similarity of genetic and phenotypic variation patterns among populations is important for making quantitative inferences about past evolutionary forces acting to differentiate populations and for evaluating the evolution of relationships among traits in response to new functional and developmental relationships. Here, phenotypic co variance and correlation structure is compared among Platyrrhine Neotropical primates. Comparisons range from among species within a genus to the superfamily level. Matrix correlation followed by Mantel's test and vector correlation among responses to random natural selection vectors (random skewers) were used to compare correlation and variance/covariance matrices of 39 skull traits. Sampling errors involved in matrix estimates were taken into account in comparisons using matrix repeatability to set upper limits for each pairwise comparison. Results indicate that covariance structure is not strictly constant but that the amount of variance pattern divergence observed among taxa is generally low and not associated with taxonomic distance. Specific instances of divergence are identified. There is no correlation between the amount of divergence in covariance patterns among the 16 genera and their phylogenetic distance derived from a conjoint analysis of four already published nuclear gene datasets. In contrast, there is a significant correlation between phylogenetic distance and morphological distance (Mahalanobis distance among genus centroids). This result indicates that while the phenotypic means were evolving during the last 30 millions years of New World monkey evolution, phenotypic covariance structures of Neotropical primate skulls have remained relatively consistent. Neotropical primates can be divided into four major groups based on their feeding habits (fruit-leaves, seed-fruits, insect-fruits, and gum-insect-fruits). Differences in phenotypic covariance structure are correlated with differences in feeding habits, indicating that to some extent changes in interrelationships among skull traits are associated with changes in feeding habits. Finally, common patterns and levels of morphological integration are found among Platyrrhine primates, suggesting that functional/developmental integration could be one major factor keeping covariance structure relatively stable during evolutionary diversification of South American monkeys.
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                Author and article information

                Journal
                EvoDevo
                EvoDevo
                BioMed Central
                2041-9139
                2011
                1 November 2011
                : 2
                : 21
                Affiliations
                [1 ]Paläontologisches Institut und Museum, Universität Zürich, Karl Schmid-Strasse 4, CH-8006 Zürich, Switzerland
                [2 ]The University Museum, The University of Tokyo, Hongo 7-3-1, Bunkyo-ku, 113-0033 Tokyo, Japan
                [3 ]Department of Biological Sciences, Vanderbilt University, VU Station B, Box 35-1634, Nashville, USA
                [4 ]Anthropologisches Institut, Universität Zürich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
                [5 ]Department of Zoology, Okayama University of Science, Ridaichou, Kita-ku, 700-0005 Okayama, Japan
                [6 ]The Second Department of Anatomy, School of Dentistry, Aichi-Gakuin University, Kusumotochou 1-100, 464-8650 Nagoya, Japan
                [7 ]Faculty of Agriculture, Tokyo University of Agriculture, Funako 1737, 243-0034 Atsugi, Japan
                Article
                2041-9139-2-21
                10.1186/2041-9139-2-21
                3247175
                22040374
                c6e232f0-eac6-4ffa-af17-bc99c631e420
                Copyright ©2011 Koyabu 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
                : 5 July 2011
                : 1 November 2011
                Categories
                Research

                Developmental biology
                micro ct,embryology,skull,integration,ossification,heterochrony,phylogeny,eulipotyphla
                Developmental biology
                micro ct, embryology, skull, integration, ossification, heterochrony, phylogeny, eulipotyphla

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