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

Abstract

Survival and divergence in a small group: the extraordinary genomic history of the endangered Apennine brown bear stragglers 2 AbstractAbout 100 km east of Rome, in the Central Apennine mountains, a critically endangered population of approximately fifty brown bears live in complete isolation. Mating outside this population is prevented by several hundred kilometers of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. First, 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 non-random 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 a) can be an important driver of divergence in isolation, b) can be tolerated when balancing selection prevents random loss of variation at important genes and c) is followed by or results directly in favorable behavioral changes. SignificanceA 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 to 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.

Genetic differentiation and asymmetric gene flow among Carpathian brown bear (Ursus arctos) populations—Implications for conservation of transboundary populations

“…This finding is consistent with Korsten et al () and Anijalg et al () who postulated that clade 3a1 experienced a widespread westward expansion after LGM across northern Eurasia and had more western distribution. Our microsatellite and mtDNA data, coupled with a recent genomic study of brown bear in Western and Central Europe (Benazzo et al, ), showed a complex scenario for the Western Carpathians. The initial colonization of the Western Carpathians by brown bears possessing mtDNA from subclade K of the Eastern lineage could have occurred during the late LGM as shown in Figure d of Anijalg et al ().…”

Genomic patterns in the widespread Eurasian lynx shaped by Late Quaternary climatic fluctuations and anthropogenic impacts

“…The sustained negative population trends during the Holocene probably contribute to the signals of recent bottlenecks, such as reduced X/A ratios and high Tajima's D values that all populations show. Additionally, even the most diverse populations show values of genetic diversity similar to that of the severely bottlenecked Apennine brown bear (Benazzo et al, ), and only twice that of the extremely eroded sister‐species—the Iberian lynx (θ = 2.22 × 10 −4 , π = 2.6 × 10 −4 ; Abascal et al, ), whose values are comparable to the least diverse Eurasian lynx populations (Figure ). Still, differences in recent demography between populations, with European populations experiencing a severe reduction in population size throughout the Holocene and Asian populations usually maintaining a softer population decline, are reflected in current genetic patterns: European populations, especially westernmost ones, show larger genetic differentiation, increased drift parameters in treemix analysis, along with bottleneck signals and lower genome diversity.…”

Mammal endemism In Italy: A review

“…This Appennine endemic subspecies appears to be deeply distinct from the other European populations from a morphological point of view (Colangelo et al 2012b), while showing a genetic affinity between the remnant and isolated population of the other southern European populations (Swenson et al, 2011). However, Benazzo et al (2017) on the basis 26 of genomic analyzes have indicated a separation of the Apennine bears, from the rest of the other bear populations, of about 1500 years. The authors conclude that Apennines bear population represents a divergent evolutionary lineage.…”