Not out of the woods yet: signatures of the prolonged negative genetic
consequences of a population bottleneck in a rapidly re-expanding wader,
the black-faced spoonbill Platalea minor
Abstract
The long-term persistence of a population which has suffered a
bottleneck partly depends on how historical demographic dynamics
impacted its genetic diversity and the accumulation of deleterious
mutations. Here we provide genomic evidence for the detrimental genetic
effect of a recent population bottleneck in the endangered black-faced
spoonbill (Platalea minor) even after its rapid population
recovery. Our population genomic data suggest that the bird’s effective
population size, Ne, had been relatively stable
(7,500-9,000) since the end of the last glacial maximum; however, a
recent brief yet severe bottleneck (Ne= 20)
around the 1940s wiped out more than 99% of its historical
Ne in roughly three generations. By comparing it
with its sister species, the royal spoonbill (P. regia) whose
conservation status is of lesser concern, we found that despite a more
than 15-fold population recovery since 1988, genetic drift has led to
higher levels of inbreeding (7.4 times more runs of homozygosity longer
than 100 Kb) in the black-faced spoonbill than in the royal spoonbill
genome. Although the two spoonbills have similar levels of genome-wide
nucleotide diversity and heterozygosity, because of relaxed purifying
selection, individual black-faced spoonbills carry 3% more
nonsynonymous substitutions than royal spoonbills each of which is 7%
more deleterious. Our results imply that the persistence of a threatened
species cannot be inferred from a recovery in its population. They also
highlight the necessity of continually using genomic indices to monitor
its genetic health and employing all possible measures to assure its
long-term persistence in the ever-changing environment.