Lifetime Fitness Costs of Inbreeding and Being Inbred in a Critically Endangered Bird

Reduced fitness as a result of inbreeding is a major threat facing many species of conservation concern. However, few case studies for assessing the magnitude of inbreeding depression in the wild means that its relative importance as a risk factor for population persistence remains under-appreciated. The increasing availability and affordability of genomic technologies provide new opportunities to address knowledge gaps around the magnitude and manifestation of inbreeding depression in wild populations. Here, we combine over three decades of individual lifetime reproductive data and genomic data to estimate the relative lifetime and short-term fitness costs of both being inbred and engaging in inbreeding in the last wild population (<250 individuals remaining) of an iconic and critically endangered bird: the helmeted honeyeater Lichenostomus melanops cassidix. The magnitude of inbreeding depression was substantial: the mean predicted lifetime reproductive success of the most inbred (homozygosity = 0.82) individuals was on average 87%–90% lower than that of the least inbred (homozygosity = 0.75). For individual reproductive events and lifetime measures, we provide rare empirical evidence that pairing with a genetically dissimilar individual can reduce fitness costs associated with being an inbred individual. By comparing lifetime and short-term fitness measures, we demonstrate how short-term measures of reproductive success that are associated with only weak signatures of inbreeding depression can still underlie stronger lifetime effects. Our study represents a valuable case study, highlighting the critical importance of inbreeding depression as a factor influencing the immediate viability of populations in threatened species management.