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.

Adult survival selection in relation to multilocus heterozygosity and body size in a tropical bird species, the Zenaida dove, Zenaida aurita

“…First, heterozygosity-fitness correlations (HFCs) are expected to be weak in natural populations (Chapman et al 2009;Szulkin et al 2010), and it has been argued that their identification would most often require the use of a much larger set of genetic markers than usual (Chapman et al 2009;Hoffman et al 2014;. However, significant correlations between various life history traits or sexually selected traits and multilocus heterozygosity (MLH) based on a limited number (<25) of microsatellites have been recently evidenced in several species (see for instance Harrison et al 2011;Agudo et al 2012;Wetzel et al 2012;Gillingham et al 2013;Cain et al 2014;Forcada and Hoffman 2014;Herdegen et al 2014), suggesting that the use of a large set of markers is not always necessary. In addition, there is evidence that, under certain circumstances, a small panel of microsatellite markers (n = 11) can produce equally strong or even stronger HFCs as a large panel of single-nucleotide polymorphism markers (Fortsmeier et al 2012).…”

Local effects drive heterozygosity–fitness correlations in an outcrossing long-lived tree

“…[22]) and the long-term maintenance of diversity [23]. Finally, the type and genome location of molecular markers used to test for HFCs have great importance, as fitness effects are expected to be different depending on whether the markers are neutral or potentially functional, and local or widespread in the genome [4,13,21,24,25]. In this context, genome-wide single nucleotide polymorphisms (SNPs) may help to overcome the inherent limitations traditionally associated to the study of HFCs [18,26,27].…”

“…Moreover, for marker loci to be able to estimate general inbreeding, the studied population must have gone through some mechanism generating variation in inbreeding, such as consanguineous matings, genetic drift or a recent bottleneck [7,21]. Rates of both local and genome-wide recombination are also relevant, as they influence the effect of selection on neighbouring neutral sites through linkage (e.g.…”

Ecological and association genetics in two Mediterranean pine species

“…Corbett-Detig et al 2015) and the long-term maintenance of diversity (Jaramillo-Correa et al 2010). Finally, the type and genome location of molecular markers used to test for HFCs have great importance, as fitness effects are expected to be different depending on whether the markers are neutral or potentially functional, and local or widespread in the genome (Da Silva et al 2009;Olano-Marin et al 2011;Szulkin and David 2011;Agudo et al 2012;Voegeli et al 2013). In this context, genome-wide Single Nucleotide Polymorphisms (SNPs) may help to overcome the inherent limitations traditionally associated to the study of HFCs (Hoffman et al 2014;.…”

“…Moreover, for marker loci to be able to estimate general inbreeding, the studied population must have gone through some mechanism generating variation in inbreeding, such as consanguineous matings, genetic drift or a recent bottleneck (Szulkin et al 2010;Agudo et al 2012). Rates of both local and genome-wide recombination are also relevant, as they influence the effect of selection on neighbouring neutral sites through linkage (e.g.…”