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).