Edited by Stephen R. Palumbi, Stanford University, Pacific Grove, CA, and approved October 3, 2017 (received for review May 30, 2017)
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.
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.
↵1A.B. and E.T. contributed equally to this work.
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.
Edited by Stephen R. Palumbi, Stanford University, Pacific Grove, CA, and approved October 3, 2017 (received for review May 30, 2017)
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.
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.
↵1A.B. and E.T. contributed equally to this work.
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.
