Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird

Abstract

There is compelling evidence about the manifest effects of inbreeding depression on individual fitness and populations' risk of extinction. The majority of studies addressing inbreeding depression on wild populations are generally based on indirect measures of inbreeding using neutral markers. However, the study of functional loci, such as genes of the major histocompatibility complex (MHC), is highly recommended. MHC genes constitute an essential component of the immune system of individuals, which is directly related to individual fitness and survival. In this study, we analyse heterozygosity fitness correlations of neutral and adaptive genetic variation (22 microsatellite loci and two loci of the MHC class II, respectively) with the age of recruitment and breeding success of a decimated and geographically isolated population of a long-lived territorial vulture. Our results indicate a negative correlation between neutral genetic diversity and age of recruitment, suggesting that inbreeding may be delaying reproduction. We also found a positive correlation between functional (MHC) genetic diversity and breeding success, together with a specific positive effect of the most frequent pair of cosegregating MHC alleles in the population. Globally, our findings demonstrate that genetic depauperation in small populations has a negative impact on the individual fitness, thus increasing the populations' extinction risk.

Figure 1.

Individual homozygosity by loci (HL; left axis, squares) and internal relatedness (IR; right axis, triangles) in individuals with two, three and four different MHC alleles. Bars show mean ±95% CI.

Figure 2.

Correlation of neutral genetic diversity (black dots, HL; white dots, IR) and age of recruitment in Canarian Egyptian vultures.

Figure 3.

The number of MHC alleles (mean and 95% CI) in relation to successful and failed breeding attempts (pooled data from the entire study period). Data for individual birds are shown by circles with continuous lines; breeding pairs are shown by triangles with dashed lines.