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Influence of Evolutionary Allometry on Rates of Morphological Evolution and Disparity in strictly Subterranean Moles (Talpinae, Talpidae, Lipotyphla, Mammalia)

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Abstract

The adaptation to a particular function could directly influence the morphological evolution of an anatomical structure as well as its rates. The humeral morphology of moles (subfamily Talpinae) is highly modified in response to intense burrowing and fully fossorial lifestyle. However, little is known of the evolutionary pathways that marked its diversification in the two highly fossorial moles tribes Talpini and Scalopini. We used two-dimensional landmark-based geometric morphometrics and comparative methods to understand which factors influenced the rates and patterns of the morphological evolution of the humerus in 53 extant and extinct species of the Talpini (22 extant plus 12 extinct) and Scalopini (six extant plus 13 extinct) tribes, for a total of 623 humeri. We first built a synthetic phylogeny of extinct and extant taxa of the subfamily Talpinae based on all the available information from known phylogenies, molecular data, and age ranges of fossil records. We tested for evolutionary allometry by means of multivariate regression of shape on size variables. Evolutionary allometric trajectories exhibited convergence of humeral shape between the two tribes, even when controlling for phylogeny, though a significant differences in the evolutionary rates was found between the two tribes. Talpini, unlike Scalopini, seem to have reached a robust fossorial morphology early during their evolution, and their shape disparity did not change, if it did not decrease, through time. Furthermore, the basal Geotrypus spp. clearly set apart from the other highly fossorial moles, exhibiting a significant acceleration of evolutionary shifts toward higher degree of fossorial adaptation. Our observations support the hypothesis that the evolution of allometry may reflect a biological demand (in this case functional) that constrains the rates of evolution of anatomical structures.

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Acknowledgements

We are particularly grateful to Dr. Lars van den Hoek Ostende of the Naturalis Biodiversitat Centre, Leiden, Netherlands, Dr. Reinhard Ziegler of the Staatliches Museum fur Naturkunde, Stuttgart, Germany, Prof. Barbara Rzebik-Kowalska of ISEZ-PAN, Krakow, Poland, and Dr. Shin-Ichiro Kawada of the Tsukuba Natural History Museum, Tsukuba, Ibaraki, Japan, for their helpful suggestions during the manuscript preparation. We wish to thank Dr. Christiane Bastos-Silvera of the Museu de Historia Natural, Lisboa, Portugal; Prof. Zhuding Qiu of IVPP, Beijing, China; Dr. Paula Jenkins, Dr. Roberto Portella and Dr. Emma Bernard of NHM, London, UK; Dr. Emmanuel Robert of Lyon Universitè, Lyon, France; Dr. Michael Rummel of Augsburg Naturmuseum, Augsburg, Germany; Dr. Gertrud Roessner of BSPG, Munich, Germany; Dr. Ursula Goelich of the Wien Natural History Museum, Wien, Austria; Dr. Jim Dines of LACM, Los Angeles, USA; Dr. Patricia Holroyd of UCMP, Berkeley, USA; Dr. Mihaly Gasparik of the Budapest Natural History Museum, Budapest, Hungary; Prof. Laszlo Kordos of the Budapest Geological Survey, Budapest, Hungary; Prof. Yukimitzu Tomida of Tokyo NHM, Tsukuba, Japan; and Dr. Paolo Agnelli of “La Specola” Museo di Storia Naturale di Firenze, Italy. They each allowed us to visit their collections and made our visits comfortable and pleasant.

We are grateful to two anonymous referee for their useful comments during the manuscript preparation.

G. Sansalone received support from the SYNTHESYS Project (http://www.synthesys.info), which is financed by the European Community Research Infrastructure Action under the FP7 “Capacities” Program (GB-TAF-2095 and AT-TAF-3415).

The research of A.A. Bannikova and E.D. Zemlemerova was financially supported by the Russian Science Foundation, project 14-50-00029, and the Russian Foundation for Basic Research, project 15-29-02771.

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Authors and Affiliations

  1. Department of Sciences, Roma Tre University, Largo San Leonardo Murialdo 1, I-00146, Rome, Italy

    G. Sansalone & T. Kotsakis

  2. Center for Evolutionary Ecology, Largo San Leonardo Murialdo 1, I-00146, Rome, Italy

    G. Sansalone, P. Colangelo, T. Kotsakis & A. Loy

  3. Form, Evolution and Anatomy Research Laboratory, Zoology, School of Environmental and Rural Sciences, University of New England, Armidale, NSW, 2351, Australia

    G. Sansalone

  4. National Research Council, Institute of Ecosystem Study, Largo Tonolli 50, 28922, Verbania Pallanza (VB), Italy

    P. Colangelo

  5. Environmetrics Lab, Dipartimento STAT, Università del Molise, I-86090, Pesche, Italy

    A. Loy

  6. Department of Biology and Biotechnology “Charles Darwin”, “Sapienza”, University of Rome, Via Borelli 50, I-00161, Rome, Italy

    R. Castiglia

  7. Lomonosov Moscow State University, Vorobyevy Gory, Moscow, 119992, Russia

    A. A. Bannikova & E. D. Zemlemerova

  8. Dipartimento di Scienze Cardiovascolari,Respiratorie, Nefrologiche, Anestesiologiche e Geriatriche, “Sapienza”, Rome, Italy

    P. Piras

  9. Dipartimento di Ingegneria Strutturale e Geotecnica, Sapienza, Università di Roma, Via Eudossiana 18, 00100, Rome, Italy Università di Roma, Via del Policlinico 155, 00161, Rome, Italy

    P. Piras

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  1. G. Sansalone
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  2. P. Colangelo
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  4. A. Loy
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  6. A. A. Bannikova
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Corresponding author

Correspondence to G. Sansalone.

Electronic supplementary material

Supplementary Table I.

List of specimens used in this study. (PDF 8 kb)

Supplementary Table II.

Number of individuals per species. (PDF 6 kb)

Supplementary Table III.

References used for species stratigraphy and phylogenetic position. (PDF 17 kb)

Supplementary Figure I.

Three-dimensional dynamic plot of the first three PC scores of the shape coordinates. Talpini (red hull); green spheres represent Geotrypus spp.; Scalopini (black hull). (XLSX 44 kb)

Supplementary Figure II.

Three-dimensional dynamic plot of the allometric trajectories of Talpini (red dots) and Scalopini (black dots). (XLSX 39 kb)

Supplementary Figure III.

Three-dimensional dynamic plot of phylomorphospace, representing ages/shapes/sizes. Ages (x-axis) are represented by the relative ages of the tips; shapes (y-axis) are represented by the first PC scores; sizes (z-axis) are represented by the centroid size (CS) values. Talpini (red dots), Scalopini (black dots). (XLSX 31 kb)

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Sansalone, G., Colangelo, P., Kotsakis, T. et al. Influence of Evolutionary Allometry on Rates of Morphological Evolution and Disparity in strictly Subterranean Moles (Talpinae, Talpidae, Lipotyphla, Mammalia). J Mammal Evol 25, 1–14 (2018). https://doi.org/10.1007/s10914-016-9370-9

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