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Strong phylogenetic constraint on transition metal incorporation in the mandibles of the hyper-diverse Hymenoptera (Insecta)

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Abstract

In several groups of insects, body structures related to feeding and oviposition are known to have a hardened cuticle by incorporation of transition metals. However, a functional link between metal enrichment and ecological pressures (i.e., adaptation) has been only rarely shown, opening the possibility that in some lineages, the evolutionary history may account for most of the observed variation (i.e., phylogenetic constraint). Here, we addressed this question in the hyper-diverse Hymenoptera (bees, wasps, ants, and sawflies), in which Zn and/or Mn have been found enriching the mandibles of a number of species. Across 87 species spanning most of the extant superfamilies, we found Zn enrichment to be widespread (57 species). Although lacking in the most primitive “Symphyta”, our ancestral state reconstruction was not conclusive in determining whether Zn enrichment was a derived state for the complete order, but it was clearly the ancestral state for the Apocrita, where it was lost in few lineages, notably in Aculeata (where it was then reacquired at least three times). Mn, on the other hand, occurred very rarely in mandibles (10 species). Our comparative analysis revealed a strong phylogenetic effect explaining most Zn % and Mn % variation in mandibles. Additionally, species with herbivorous larvae were less prone to have Zn (but not Mn) than those with carnivorous larvae, although a causal effect of diet on this trait was unlikely. Furthermore, species emerging from concealed vs. unconcealed development sites have similar likelihood to have metal-enriched mandibles. Evolutionary history seems to constrain metal enrichment in hymenopteran mandibles, yet the few observed losses and regains of this trait during evolution claim for deeper investigations on the role of alternative, here untested, ecological pressures.

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Acknowledgments

Thanks are due to Mercedes Paris (MNCN, CSIC) for support in selecting the individuals from the museum collection.

Funding

The study was funded by a SECTI post-doctoral contract from the Universidad de Castilla-La Mancha (to CP), by a SYNTHESYS grant from the European Union (ES-TAF 5333) (to CP), and by the following funded projects from Ministerio de Economía, Industria y Competitividad (España): CGL2017-83046-P (to CP and CO) and CGL2010-16730 (to JT and JDA).

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  1. Instituto de Ciencias Ambientales (ICAM), Universidad de Castilla-La Mancha, Avenida Carlos III, s/n, E-45071, Toledo, Spain

    Carlo Polidori

  2. Laboratorio de Microscopia, Museo Nacional de Ciencias Naturales (CSIC), C/ José Gutiérrez Abascal 2, ES-28006, Madrid, Spain

    Alberto Jorge

  3. Center for Computational and Theoretical Biology, University of Wuerzburg, Hubland Nord, 97074, Würzburg, Germany

    Alexander Keller

  4. Department of Bioinformatics, University of Wuerzburg, Am Hubland, 97074, Würzburg, Germany

    Alexander Keller

  5. Departamento de Biodiversidad, Ecología y Evolución, Universidad Complutense de Madrid, C/ José Antonio Nováis, 12, 28040, Madrid, Spain

    Concepción Ornosa

  6. Unidad de Zoología, Facultad de Biología, Universidad de Salamanca, 37071, Salamanca, Spain

    José Tormos & Josep Daniel Asís

  7. Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), C/ José Gutiérrez Abascal 2, ES-28006, Madrid, Spain

    José Luis Nieves-Aldrey

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Polidori, C., Jorge, A., Keller, A. et al. Strong phylogenetic constraint on transition metal incorporation in the mandibles of the hyper-diverse Hymenoptera (Insecta). Org Divers Evol 20, 511–526 (2020). https://doi.org/10.1007/s13127-020-00448-x

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