Genetic Signatures of Demographic Changes in an Avian Top Predator during the Last Century: Bottlenecks and Expansions of the Eurasian Eagle Owl in the Iberian Peninsula

Abstract

The study of the demographic history of species can help to understand the negative impact of recent population declines in organisms of conservation concern. Here, we use neutral molecular markers to explore the genetic consequences of the recent population decline and posterior recovery of the Eurasian eagle owl (Bubo bubo) in the Iberian Peninsula. During the last century, the species was the object of extermination programs, suffering direct persecution by hunters until the 70's. Moreover, during the last decades the eagle owl was severely impacted by increased mortality due to electrocution and the decline of its main prey species, the European rabbit (Oryctolagus cuniculus). In recent times, the decrease of direct persecution and the implementation of some conservation schemes have allowed the species' demographic recovery. Yet, it remains unknown to which extent the past population decline and the later expansion have influenced the current species' pattern of genetic diversity. We used eight microsatellite markers to genotype 235 eagle owls from ten Spanish subpopulations and analyse the presence of genetic signatures attributable to the recent population fluctuations experienced by the species. We found moderate levels of differentiation among the studied subpopulations and Bayesian analyses revealed the existence of three genetic clusters that grouped subpopulations from central, south-western and south-eastern Spain. The observed genetic structure could have resulted from recent human-induced population fragmentation, a patchy distribution of prey populations and/or the philopatric behaviour and habitat selection of the species. We detected an old population bottleneck, which occurred approximately 10,000 years ago, and significant signatures of recent demographic expansions. However, we did not find genetic signatures for a recent bottleneck, which may indicate that population declines were not severe enough to leave detectable signals on the species genetic makeup or that such signals have been eroded by the rapid demographic recovery experienced by the species in recent years.

Fig 1. Distribution of the Eurasian eagle owl (Bubo bubo) in the Iberian Peninsula.

This species can be considered continuous across the Iberian Peninsula, with the exception of the coastal region in the center and north of Portugal, and Galicia and the Cantabrian coasts in Spain. The number of analysed chicks (N) in each subpopulation is indicated.

Fig 2. Genetic assignment of individuals based on the Bayesian method implemented in the program Structure.

The number of inferred clusters was fixed to three, as this represents the most supported value of K. The admixture proportions generated by the software were represented using pie charts for each studied subpopulation, with each colour indicating a different genotypic cluster. Each individual is represented by a thin vertical bar, which is partitioned into coloured segments that represent the individual’s probability of belonging to the cluster with that colour.

Fig 3. Spatial clustering analysis in Geneland.

The number of inferred clusters was fixed to three, as this represents the most supported value of K. The admixture proportions for each studied subpopulation were represented using pie charts, with each colour indicating a different genotypic cluster.

Fig 4. Inference of the demographic history of the Eurasian eagle owl (Bubo bubo) in Spain.

Results obtained from the analyses with Msvar 1.3. Solid lines correspond to the posterior distribution of the parameters obtained in the five different runs. The wide uninformative priors employed in the analyses are represented by the dashed lines. (a) Posterior distribution of ancestral (N1) and present (N0) population effective sizes. (b) Posterior distribution of the time (in years ago) since the population collapse.

Fig 5. Eagle owl distance recoveries in Spain during the period 1973–2010.

No differences were detected between bird ringed as chicks or juveniles (Euring 1 and 3) and adults (Pearson's Chi-squared test, χ₈ ² = 7.31, p = 0.503, n = 206).