Tuberculosis susceptibility and inbreeding depression hinder ex-situ conservation in a critically endangered rainforest bird

Abstract

Captive breeding can be a key component of species conservation strategies, but also exposes these rare species to novel environments including the pathogen landscape. The critically endangered white-winged wood duck (WWWD) Asarcornis scutulata has experienced substantial population declines, local extirpations and fragmentation of its former range in South-East Asia, making it one of the rarest birds in the world. Like other rare species, WWWD declines have led to the initiation of captive breeding programs, but these have been hampered by the WWWDs high susceptibility to Mycobacterium avium, avian tuberculosis (TB). In this study we describe genome-wide patterns of diversity to understand the WWWDs demographic and phylogeographic history, inbreeding in the wild and in captivity, and the causes of TB susceptibility. Captive birds, which originated from northeast India, are genetically differentiated from wild birds sampled in Sumatra, Indonesia, likely reflecting long-standing phylogeographic structure. Demographic analyses revealed that long-term (Pleistocene) population declines preceded anthropogenic declines, a pattern shared with other codistributed, forest-dependent species. All sampled WWWD populations had extremely low genetic diversity but wild-sampled birds retained higher Major Histocompatibility Complex (MHC) diversity, reflecting important functional diversity in the wild. Genetic diversity has eroded over time in captivity and importantly, birds with higher levels of inbreeding succumb earlier to TB infections, suggesting inbreeding depression. Finally, by comparing gene expression between susceptible WWWD and resistant redhead ducks Aythya americana we identify possible mechanisms of TB susceptibility in WWWD. Altogether our study provides genomically-guided objectives for future management and a cautionary tale for ex-situ conservation.