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A Dysfunctional Sense of Smell: The Irreversibility of Olfactory Evolution in Free-Living Pigs

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Abstract

Artificial selection began to override natural selection in domesticated wild boar and other species about 10,000 years ago. The intentional selection of a desired phenotypic trait is a complex process, and comes along with unexpected or even unwanted changes in other traits, because of epistatic gene effects, and ontogenetic constraints. The loss of brain mass in domestic ungulates is related to selection for reduced reaction to external stimuli. Evolutionary losses in body structures and genes were once considered mostly irreversible, in keeping with Dollo’s law. Here we studied the biochemical and the histological functioning of the free-living pigs (FLPs) olfactory system, to see if and to what extent does FLPs regain a full sense of smell, as compared to the domestic pigs and wild boar Sus scrofa. In our samples both wild boars and FLPs have significantly larger brain per unit mass than domestic pigs, and FLPs’ brains are not significantly smaller than wild boar’s. Similarly, both wild boars and FLPs have significantly higher cell density than domestic pigs in the olfactory mucosa. Yet, at the functional level, olfactory marker protein and neuropeptide Y, both of which are important to the correct functioning of the sense of smell, are fully expressed only in wild boar. These results suggest that FLPs reacquired structural, but not the biochemical capability in their olfactory system.

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Acknowledgments

We are grateful to Daniele Carrada for assistance in the sampling and Gian Carlo Carrada for their constructive comments in preparing the manuscript. This work was supported by Department of Biology University of Naples Federico II, the Cilento e Vallo di Diano e degli Alburni National Park, and Ambito Territoriale di Caccia delle Aree Contigue al Parco Nazionale del Cilento e Vallo di Diano.

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Authors and Affiliations

  1. Department of Environmental Biological and Pharmaceutical Sciences and Technologies, Second University of Naples SUN, Via Vivaldi 48, 81100, Caserta, Italy

    Valeria Maselli & Roberto Ligrone

  2. Department of Biology, University of Naples Federico II, Campus Monte S. Angelo, 80126, Naples, Italy

    Valeria Maselli, Gianluca Polese, Nicola Forte, Daniela Rippa, Rosario Vicidomini & Domenico Fulgione

  3. Durham Evolution and Ancient DNA, Department of Archaeology, University of Durham, Durham, DH1 3LE, UK

    Greger Larson

  4. Department of Earth Sciences, Resources and Environment, University of Naples Federico II, Largo San Marcellino 10, 80138, Naples, Italy

    Pasquale Raia

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  1. Valeria Maselli
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  2. Gianluca Polese
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  3. Greger Larson
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  4. Pasquale Raia
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  9. Domenico Fulgione
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Correspondence to Domenico Fulgione.

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Valeria Maselli and Gianluca Polese have contributed equally to this study.

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Maselli, V., Polese, G., Larson, G. et al. A Dysfunctional Sense of Smell: The Irreversibility of Olfactory Evolution in Free-Living Pigs. Evol Biol 41, 229–239 (2014). https://doi.org/10.1007/s11692-013-9262-3

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