Demographic history, not mating system, explains signatures of inbreeding and inbreeding depression in a large outbred population

Abstract

Inbreeding depression is often found in small, inbred populations, but whether it can be detected in and have evolutionary consequences for large, wide-ranging populations is poorly known. Here, we investigate the possibility of inbreeding in a large population to determine whether mild levels of inbreeding can still have genetic and phenotypic consequences and how genomically widespread these effects can be. We apply genome-wide methods to investigate whether individual and parental heterozygosity is related to morphological, growth, or life-history traits in a pelagic seabird, Leach’s storm-petrel (Oceanodroma leucorhoa). Examining 560 individuals as part of a multiyear study, we found a substantial effect of maternal heterozygosity on chick traits: chicks from less heterozygous (relatively inbred) mothers were significantly smaller than chicks from more heterozygous (noninbred) mothers. We show that these heterozygosity-fitness correlations were due to general genome-wide effects and demonstrate a correlation between heterozygosity and inbreeding, suggesting inbreeding depression. We used population genetic models to further show that the variance in inbreeding was probably due to past demographic events rather than the current mating system and ongoing mate choice. Our findings demonstrate that inbreeding depression can be observed in large populations and illustrate how the integration of genomic techniques and fieldwork can elucidate its underlying causes.