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Research Article

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

Andrea Benazzo, Emiliano Trucchi, James A. Cahill, Pierpaolo Maisano Delser, Stefano Mona, Matteo Fumagalli, View ORCID ProfileLynsey Bunnefeld, Luca Cornetti, Silvia Ghirotto, Matteo Girardi, Lino Ometto, Alex Panziera, Omar Rota-Stabelli, Enrico Zanetti, Alexandros Karamanlidis, Claudio Groff, Ladislav Paule, Leonardo Gentile, View ORCID ProfileCarles Vilà, Saverio Vicario, Luigi Boitani, View ORCID ProfileLudovic Orlando, Silvia Fuselli, Cristiano Vernesi, View ORCID ProfileBeth Shapiro, View ORCID ProfilePaolo Ciucci, and Giorgio Bertorelle
  1. aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
  2. bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo 1066, Norway;
  3. cDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
  4. dInstitute de Systematics, Evolution, Biodiversite, UMR 7205-CNRS, Muséum National d'Histoire Naturelle, Université Pierre et Marie Curie, École Pratique des Hautes Études (EPHE), CP39, 75005 Paris, France;
  5. eEPHE, Paris Sciences & Lettres Research University, 75005 Paris, France;
  6. fSmurfit Institute of Genetics, Trinity College, University of Dublin, Dublin 2, Ireland;
  7. gDepartment of Life Sciences, Imperial College London, Ascot SL5 7PY, United Kingdom;
  8. hInstitute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, United Kingdom;
  9. iBiological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, United Kingdom;
  10. jZoological Institute, University of Basel, 4051 Basel, Switzerland;
  11. kDepartment of Biodiversity and Molecular Ecology, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy;
  12. lDepartment of Sustainable Agro-Ecosystems and Bioresources, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy;
  13. mIndependent Researcher, 38016 Mezzocorona, Italy;
  14. nProtection and Management of Wildlife and the Natural Environment, ARCTUROS, 53075 Aetos, Florina, Greece;
  15. oForest and Wildlife Service, Provincia Autonoma di Trento, 38100 Trento, Italy;
  16. pDepartment of Phytology, Faculty of Forestry, Technical University, 96053 Zvolen, Slovakia;
  17. qVeterinary Service, National Park of Abruzzo Lazio and Molise, 67032 Pescasseroli, Italy;
  18. rDepartment of Integrative Ecology, Doñana Biological Station, Consejo Superior de Investigaciones Científicas, 4102 Seville, Spain;
  19. sInstitute of Atmospheric Pollution Research and Technologies, National Research Council, 70126 Bari, Italy;
  20. tDepartment of Biology and Biotechnologies “Charles Darwin,” University of Rome La Sapienza, 00185 Rome, Italy;
  21. uCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350 K Copenhagen, Denmark

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PNAS November 7, 2017 114 (45) E9589-E9597; first published October 24, 2017; https://doi.org/10.1073/pnas.1707279114
Andrea Benazzo
aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
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Emiliano Trucchi
aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
bCentre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo 1066, Norway;
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James A. Cahill
cDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
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Pierpaolo Maisano Delser
dInstitute de Systematics, Evolution, Biodiversite, UMR 7205-CNRS, Muséum National d'Histoire Naturelle, Université Pierre et Marie Curie, École Pratique des Hautes Études (EPHE), CP39, 75005 Paris, France;
eEPHE, Paris Sciences & Lettres Research University, 75005 Paris, France;
fSmurfit Institute of Genetics, Trinity College, University of Dublin, Dublin 2, Ireland;
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Stefano Mona
dInstitute de Systematics, Evolution, Biodiversite, UMR 7205-CNRS, Muséum National d'Histoire Naturelle, Université Pierre et Marie Curie, École Pratique des Hautes Études (EPHE), CP39, 75005 Paris, France;
eEPHE, Paris Sciences & Lettres Research University, 75005 Paris, France;
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Matteo Fumagalli
gDepartment of Life Sciences, Imperial College London, Ascot SL5 7PY, United Kingdom;
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Lynsey Bunnefeld
hInstitute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, United Kingdom;
iBiological and Environmental Sciences, University of Stirling, Stirling FK9 4LA, United Kingdom;
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  • ORCID record for Lynsey Bunnefeld
Luca Cornetti
jZoological Institute, University of Basel, 4051 Basel, Switzerland;
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Silvia Ghirotto
aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
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Matteo Girardi
kDepartment of Biodiversity and Molecular Ecology, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy;
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Lino Ometto
lDepartment of Sustainable Agro-Ecosystems and Bioresources, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy;
mIndependent Researcher, 38016 Mezzocorona, Italy;
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Alex Panziera
aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
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Omar Rota-Stabelli
lDepartment of Sustainable Agro-Ecosystems and Bioresources, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy;
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Enrico Zanetti
aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
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Alexandros Karamanlidis
nProtection and Management of Wildlife and the Natural Environment, ARCTUROS, 53075 Aetos, Florina, Greece;
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Claudio Groff
oForest and Wildlife Service, Provincia Autonoma di Trento, 38100 Trento, Italy;
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Ladislav Paule
pDepartment of Phytology, Faculty of Forestry, Technical University, 96053 Zvolen, Slovakia;
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Leonardo Gentile
qVeterinary Service, National Park of Abruzzo Lazio and Molise, 67032 Pescasseroli, Italy;
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Carles Vilà
rDepartment of Integrative Ecology, Doñana Biological Station, Consejo Superior de Investigaciones Científicas, 4102 Seville, Spain;
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  • ORCID record for Carles Vilà
Saverio Vicario
sInstitute of Atmospheric Pollution Research and Technologies, National Research Council, 70126 Bari, Italy;
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Luigi Boitani
tDepartment of Biology and Biotechnologies “Charles Darwin,” University of Rome La Sapienza, 00185 Rome, Italy;
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Ludovic Orlando
uCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, 1350 K Copenhagen, Denmark
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  • ORCID record for Ludovic Orlando
Silvia Fuselli
aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
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Cristiano Vernesi
kDepartment of Biodiversity and Molecular Ecology, Fondazione Edmund Mach, 38010 San Michele all’Adige, Italy;
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Beth Shapiro
cDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
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Paolo Ciucci
tDepartment of Biology and Biotechnologies “Charles Darwin,” University of Rome La Sapienza, 00185 Rome, Italy;
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Giorgio Bertorelle
aDepartment of Life Sciences and Biotechnology, University of Ferrara, 44121 Ferrara, Italy;
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  • For correspondence: ggb@unife.it
  1. Edited by Stephen R. Palumbi, Stanford University, Pacific Grove, CA, and approved October 3, 2017 (received for review May 30, 2017)

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Significance

A small and relict population of brown bears lives in complete isolation in the Italian Apennine Mountains, providing a unique opportunity to study the impact of drift and selection on the genomes of a large endangered mammal and reconstruct the phenotypic consequences and the conservation implications of such evolutionary processes. The Apennine bear is highly inbred and harbors very low genomic variation. Several deleterious mutations have been accumulated by drift. We found evidence that this is a consequence of habitat fragmentation in the Neolithic, when human expansion and land clearance shrank its habitat, and that retention of variation at immune system and olfactory receptor genes as well as changes in diet and behavior prevented the extinction of the Apennine bear.

Abstract

About 100 km east of Rome, in the central Apennine Mountains, a critically endangered population of ∼50 brown bears live in complete isolation. Mating outside this population is prevented by several 100 km of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. We found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show nonrandom peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles (i) can be an important driver of divergence in isolation, (ii) can be tolerated when balancing selection prevents random loss of variation at important genes, and (iii) is followed by or results directly in favorable behavioral changes.

  • balancing selection
  • genetic drift
  • genetic load
  • Ursus arctos
  • Neolithic impact

Footnotes

  • ↵1A.B. and E.T. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: ggb{at}unife.it.
  • Author contributions: A.B., E.T., L. Boitani, P.C., and G.B. designed research; J.A.C., M.G., A.K., C.G., L.P., L.G., C. Vilà, S.F., C. Vernesi, and G.B. performed research; A.B., E.T., J.A.C., P.M.D., S.M., M.F., L. Bunnefeld, L.C., S.G., L. Ometto, A.P., O.R.-S., E.Z., S.V., L. Orlando, S.F., and G.B. analyzed data; A.K., C.G., L.P., L.G., and C. Vilà provided samples; and E.T., B.S., P.C., and G.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in GenBank's sequence read archive (accession nos. PRJNA395974 and MF593957–MF593987).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1707279114/-/DCSupplemental.

Published under the PNAS license.

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Extreme genomic effects in a small bear population
Andrea Benazzo, Emiliano Trucchi, James A. Cahill, Pierpaolo Maisano Delser, Stefano Mona, Matteo Fumagalli, Lynsey Bunnefeld, Luca Cornetti, Silvia Ghirotto, Matteo Girardi, Lino Ometto, Alex Panziera, Omar Rota-Stabelli, Enrico Zanetti, Alexandros Karamanlidis, Claudio Groff, Ladislav Paule, Leonardo Gentile, Carles Vilà, Saverio Vicario, Luigi Boitani, Ludovic Orlando, Silvia Fuselli, Cristiano Vernesi, Beth Shapiro, Paolo Ciucci, Giorgio Bertorelle
Proceedings of the National Academy of Sciences Nov 2017, 114 (45) E9589-E9597; DOI: 10.1073/pnas.1707279114

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Extreme genomic effects in a small bear population
Andrea Benazzo, Emiliano Trucchi, James A. Cahill, Pierpaolo Maisano Delser, Stefano Mona, Matteo Fumagalli, Lynsey Bunnefeld, Luca Cornetti, Silvia Ghirotto, Matteo Girardi, Lino Ometto, Alex Panziera, Omar Rota-Stabelli, Enrico Zanetti, Alexandros Karamanlidis, Claudio Groff, Ladislav Paule, Leonardo Gentile, Carles Vilà, Saverio Vicario, Luigi Boitani, Ludovic Orlando, Silvia Fuselli, Cristiano Vernesi, Beth Shapiro, Paolo Ciucci, Giorgio Bertorelle
Proceedings of the National Academy of Sciences Nov 2017, 114 (45) E9589-E9597; DOI: 10.1073/pnas.1707279114
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