Increasing fluctuating asymmetry in the isolated and highly endangered Marsican brown bear (Ursus arctos marsicanus) .

Introduction Deviations from the bilateral symmetry can be observed in some Vertebrate species as an adaptive response to specific functional demands, as the directional asymmetry of dolphin skulls. However, random fluctuations from perfect symmetry, i.e. fluctuating asymmetry, can be driven by factors not linked to the ecology or evolutionary history of the species. Specifically, fluctuating asymmetry (FA) has been hypothesized to occur when genetic and/or environmental factors produce an alteration of the developmental processes. It is the case of small and isolated populations with high level of inbreeding, where the emergence of recessive alleles can produce higher level of fluctuating asymmetry with respect to larger populations. We aimed at investigating if FA can be detected in the critically endangered, small and isolated population of the Marsican brown bear, Ursus arctos marsicanus, surviving in the Italian Central Apennines. The observed heterozygosis at microsatellite loci of the Marsican brown bear did not recognize a severe inbreeding. However, last genomic analyses posed the attention on the presence of mutations that in human are considered deleterious. Methods We analyzed 74 skulls belonging to brown bear populations of different size and degree of isolation: the smallest and most isolated Apennine (n=32), the medium sized Scandinavian (n=31), and the large Russian (n=12) population. Skulls were analyzed by means of 3D geometric morphometrics from 3D digital surface images reconstructed from either computer tomography (CT) or photogrammetry. Three replicates of 39 3D landmarks were recorded on each skull using Meshlab. After a generalized Procrustes analysis, the aligned configurations were analysed for deviation from bilateral symmetry in terms of FA compared among the three populations, using a Procrustes ANOVA in MorphoJ. Results Results showed that FA was a significant component of all populations analysed. However, the Apennine brown bear showed double levels of FA (Find×side: 7.49; p<0.0001) with respect to both the Scandinavian Find×side: 3.01; p< 0.0001) and the Russian (Find×side: 4.17; p<0.0001) samples. Discussion Our results show that the cranial distinctiveness of the small and highly endangered Apennine brown bear is coupled with a high FA level. This would suggest that the Marsican brown bear is undergoing an alteration of developmental patterns likely due to inbreeding or to the fast genetic drift experienced during the last century. This result shows that FA could represents a valuable tool to assess the ontogenetic alterations in isolated and/or endangered species by the analyse of historical series (i.e. museum specimens) giving also a contribute to a better understanding of the role developmental process modification in the evolution of small populations.