An elevated level of inbreeding in the black-faced spoonbill
Small populations are particularly prone to an elevated level of inbreeding, the mating between relatives, which can increase homozygosity at loci that carry deleterious recessive mutations and thus reduce the fitness of offspring (Crow & Kimura, 1970) (i.e. inbreeding depression). Two lines of evidence reveal the genomic footprints of inbreeding during the bottleneck and possibly the post-bottleneck period in the black-faced spoonbill population. A recent and severe bottleneck event is expected to result in an increase in the number (NROH) and length (SROH) of runs of homozygosity, which are identical homologous genomic segments(McQuillan et al., 2008). We found that the black-faced spoonbill had approximately 7.4 times the SROH (t test= -12.68,p < 0.0001) and 6.2 times the NROH (t test= -22.78, p < 0.0001) of the royal spoonbill (Fig. 3A; Table S7): the black-faced spoonbill had an average NROH of 426.42± 49.65 and average SROH of 84,154.15± 19,442.36 Kb; by contrast, the royal spoonbill had an average NROH of 68.89± 19.21 and an average SROH of 11361.82± 3645.35 Kb. In both species, most of the ROHs were less than 500 Kb long (84.6% and 90.4% of SROH for the black-faced and royal spoonbill, respectively; 96.3% and 97.6% of NROH for the black-faced and royal spoonbills, respectively), yet significantly longer ROHs (> 2,000 Kb) were observed in two black-faced spoonbills with the longest being 3,566.6 Kb. The genomic inbreeding coefficient, F ROH, which measures the fraction of the autosomal genome in ROH ( Keller, Visscher, & Goddard, 2011), was approximately seven times higher in the black-faced spoonbill than in the royal spoonbill (mean F ROH= 0.071 and 0.001 for the black-faced and royal spoonbills, respectively), but lower than those of other threatened populations (e.g. F ROH= 0.4 in the grey wolf (Gómez‐Sánchez et al., 2018)). This may reflect alleviated inbreeding due to the rapid population recovery. Moreover, inbreeding could also lead to a higher level of homozygosity and slower decay in linkage disequilibrium (Slatkin, 2008) which can be measured by the association of occurrence of alleles at two loci, expressed as a correlation coefficient (r 2). In this case,r 2 decay was slower in the black-faced spoonbill than in the royal spoonbill (Fig. 3B).