Evolutionary genomics: Fifty bear stragglers in Italy resist genomic meltdown

New publication in PNAS with first authors from University of Ferrara, Italy, and CEES at IBV, University of Oslo, Norway.

Full size images: 1 and 2.

Press release.

In Central Italy, one hundred kilometers from Rome, a small group of 50 brown bears lives in complete isolation. A study published today in PNAS, based on whole genome sequencing, reveals an extraordinary and complex history of population decline and isolation, random accumulation of deleterious mutations, active maintanance of variation at immune and olfactory genes, and morphological and behavioural divergence.  

Genomic data suggest that bears in Europe lost connectivity about 3-4,000 years ago, when early farmers burnt forests for land clearing. “This was a large scale human-mediated environmental change”, says Giorgio Bertorelle, the coordinator of this study at the University of Ferrara, “which left profound signatures on several species, as the fragmentation of a large European brown bear population and its local demographic collapse in Central Italy”.

“A consequence of this collapse” adds Andrea Benazzo, “is the desolating landscape of extremely low genetic variation observed in the Apennine bear, charaterized also by several potentially deleterious mutations shared by all the analyzed individuals and rarely found in other populations”. These are the negative effects produced by chance (random genetic drift) in small populations and are considered as the main drivers of extinction. Loss of genetic diversity is also particularly harmful if a population faces  fast environmental changes. So, the question is: how could the Apennine bears have resisted for such a long time at very low population size and be apparently in good shape?

“Surprisingly, few genomic regions with very high diversity stand out from the low and flat background characterizing the rest of the genome” says Emiliano Trucchi. These regions, whose variation can be as high as in other European bears, are enriched for immunity and olfactory receptor genes. The authors believe this is evidence of an active process maintaining high genetic diversity where variation is mostly needed, i.e. at genes responsible for the complex interactions with the external environment both as defence from pathogens and as perception of smells. Balancing selection, a special form of natural selection favouring individuals with two different copies (ie. alleles) of the same gene, seems the most likely explanation.

This study also shows that random fixation of rare and usually disadvantageous mutations can produce interesting evolutionary outcomes in small populations, such as smaller size and reduced aggressiveness. In particular, the authors discovered in the Apennine bear a significant divergence at genes that were associated with a shift to a more docile behaviour in other mammal species. Such mutations, likely accumulated by chance, could have produced the less aggressive behaviour often observed in the Apennine bear. “Attacks on men are not recorded in historic times”, says Paolo Ciucci from the University of Rome “La Sapienza”, “and this rather docile behaviour may have prevented persecution and eradication by local human communities”. In other words, it seems that the diffusion of some mutations, although clearly disadvantageous in other circumstances, could have turned into a bless for the Apennine bear.

In conclusion, the Apennine bear seems to have some cards to resist and keep fighting its evolutionary battle against genomic meltdown, despite the extremely small population size and the clear genetic consequences of their long history of inbreeding, “The endangered Apennine bears requires constant monitoring, but it also represents a beautiful natural experiment that teaches us a lot about the delicate balance between natural selection and chance in small populations”, concludes Giorgio Bertorelle.

Contact: Giorgio Bertorelle, Department of Life Sciences and Biotechnology,  University of Ferrara, Italy,  ggb@unife.it. Now at Griffith University, Brisbane, Australia. Phone: +61 478 059 203.

Original article: 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 (2017) Survival and divergence in a small group: the extraordinary genomic history of the endangered Apennine brown bear stragglers. Proceedings of the National Academy of Science USA. Doi: 10.1073/pnas.1707279114 . Link to publication webpage. *Co-first authors.

Published Oct. 27, 2017 2:22 PM - Last modified Oct. 27, 2017 2:22 PM