Scope for genetic rescue of an endangered subspecies though re-establishing natural gene flow with another subspecies.

Genetic diversity is positively linked to the viability and evolutionary potential of species but is often compromised in threatened taxa. Genetic rescue by gene flow from a more diverse or differentiated source population of the same species can be an effective strategy for alleviating inbreeding depression and boosting evolutionary potential. The helmeted honeyeater Lichenostomus melanops cassidix is a critically endangered subspecies of the common yellow-tufted honeyeater. Cassidix has declined to a single wild population of ~130 birds, despite being subject to intensive population management over recent decades. We assessed changes in microsatellite diversity in cassidix over the last four decades and used population viability analysis to explore whether genetic rescue through hybridization with the neighbouring Lichenostomus melanops gippslandicus subspecies constitutes a viable conservation strategy. The contemporary cassidix population is characterized by low genetic diversity and effective population size (N(e) < 50), suggesting it is vulnerable to inbreeding depression and will have limited capacity to evolve to changing environments. We find that gene flow from gippslandicus to cassidix has declined substantially relative to pre-1990 levels and argue that natural levels of gene flow between the two subspecies should be restored. Allowing gene flow (~4 migrants per generation) from gippslandicus into cassidix (i.e. genetic rescue), in combination with continued annual release of captive-bred cassidix (i.e. demographic rescue), should lead to positive demographic and genetic outcomes. Although we consider the risk of outbreeding depression to be low, we recommend that genetic rescue be managed within the context of the captive breeding programme, with monitoring of outcomes.

A novel framework for evaluating in situ breeding management strategies in endangered populations.

Conservation breeding management aims to reduce inbreeding and maximize the retention of genetic diversity in endangered populations. However, breeding management of wild populations is still rare, and there is a need for approaches that provide data-driven evidence of the likelihood of success of alternative in situ strategies. Here, we provide an analytical framework that uses in silico simulations to evaluate, for real wild populations, (i) the degree of population-level inbreeding avoidance, (ii) the genetic quality of mating pairs, and (iii) the potential genetic benefits of implementing two breeding management strategies. The proposed strategies aim to improve the genetic quality of breeding pairs by splitting detrimental pairs and allowing the members to re-pair in different ways. We apply the framework to the wild population of the Critically Endangered helmeted honeyeater by combining genomic data and field observations to estimate the inbreeding (i.e., pair-kinship) and genetic quality (i.e., Mate Suitability Index) of all mating pairs for seven consecutive breeding seasons. We found no evidence of population-level inbreeding avoidance and that ~91.6% of breeding pairs were detrimental to the genetic health of the population. Furthermore, the framework revealed that neither proposed management strategy would significantly improve the genetic quality or reduce inbreeding of the mating pairs in this population. Our results demonstrate the usefulness of our analytical framework for testing the efficacy of different in situ breeding management strategies and for making evidence-based management decisions.

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 [1-4]. 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 [5]. 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 [6-12]. 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.