Discussion
Relatively stable post-LGM demography
The historical demographic trajectory retrieved from population genomic
data (Fig. 2A) suggests that the N e of the this
once critically endangered species is much larger than any census global
population sizes since 1988, and was stable for most of its recent
evolutionary histories, unperturbed by the drastic climatic changes
since the end of the LGM. The large and stable historicalN e of the black-faced faced spoonbill is
consistent with the fact that its genome-wide genetic diversity
(π and mean individual heterozygosity) is similar to that of the
royal spoonbill which also had a similar post-LGM demographic trajectory
(Fig. 2A).
Another line of evidence which supports the historical abundance of the
black-faced spoonbill as documented in early literature (La Touche,
1931; Austin, 1948) is the fact that that its estimated long-termNe could be translated, assuming a simple
one-to-ten rule for the ratio between Ne and the
census breeding population size (Frankham, 1995), into over 74,200
breeding individuals. This is comparable to the similarly deduced
long-term breeding population size of the royal spoonbill of 78,000
individuals and to the current population size of royal spoonbills
(25,000-100,000 individuals; Matheu & del Hoyo, 1992). A stable and
large long-term Ne rules out the possibility that
the bottleneck observed in 1988 was the result of the long term
population decline driven by climate change since the LGM as in the case
of other endangered species (Mays et al., 2018; Li et al., 2014; Cho et
al., 2013; Zhao et al., 2013).
Could DDT have been the cause of recent population bottleneck?
Although we cannot ascertain the cause of this recent bottleneck, its
estimated start coincides with the period of the widespread use of
organochlorine pesticides (e.g. DDT) around the world, including East
Asia (Wong, Leung, Chan, & Choi, 2005), after World War II. DDT and its
metabolites are known to impair the reproduction of avian species by
thinning eggshells and acting as estrogen blockers (Cooke, 1973;
Risebrough, 1986). DDT-induced population crashes have been documented
in several raptors (Poole, 1989; Newton & Wyllie, 1992); eggshells of
other Ciconiformes species (Faber & Hickey, 1973; King, Meeker, &
Swineford, 1980) were found to thin significantly in the presence of
even a miniscule amount of DDT. Furthermore, the black-faced spoonbill
is one of the top predator species in its major wintering habitat, the
estuaries, which are known to be repositories of contaminants (Ridgway
& Shimmield, 2002) where biomagnification through the food chain would
expose the bird to a level of DDT and its metabolites higher than that
found in the environment. The adverse effects of DDT on wildlife
eventually led to its ban around the world (e.g. in 1972 by the United
States), and has been associated with the rapid recovery of some raptors
(Grier, 1982). The bottleneck event of the black-faced spoonbill was
estimated to have ended two to three generations ago, which is around
1970-1980s, consistent with the prohibition of the use of DDT in East
Asia in the 1980s (China in 1983, South Korea in 1986, and Taiwan in
1987) and the black-faced spoonbill’s population growth trend since
1988.
The recent bottleneck event experienced by the black-faced spoonbill
was, although brief, extremely severe: the N eduring the bottleneck period was estimated to be only 20 individuals
(95% CI: 12.5-47.5 individuals), roughly equivalent to 200 breeding
individuals. By contrast, the pre-bottleneck N ewas estimated to be 5491.5 (95% CI: 4549.5– 12310.5 individuals),
close to the recent historical N e (7,432)
estimated by SMC++ . In other words, more than 99% ofN e vanished during the bottleneck event. Although
the N e of the black-faced spoonbill has since
increased to 236.5 (95% CI: 57.6 – 376.0), it is still only about 4%
of its pre-bottleneck N e. The magnitude ofN e reduction would rule out the Korean War as a
candidate cause of population decline (Matheu & del Hoyo, 1992) since
the uninhabited rocky islets where the bird breeds would hardly have
been major military targets.
The questionable long-term persistence of the black-faced spoonbill
The rapid population recovery of the black-faced spoonbill may preclude
the risk of immediate extinction, although whether its currentN e of 405 could support the species’ long-term
persistence remains questionable, as it has been suggested that a
minimum N e of 1,000 is required to ensure the
evolutionary potential and long-term persistence of a population
(Frankham, Bradshaw, & Brook, 2014). Moreover, the coastal wetlands of
East Asia are under unprecedented pressure of reclamation, urbanization
and industrialization (Larson, 2015). For example, a seawall in China
which encloses its coastal wetland to support rapid urbanization and
economic development reached 11,000 km (70% of mainland China’s
coastline) in 2010 (Ma et al., 2014), fundamentally altering the coastal
ecosystem and inevitably reducing the environmental carrying capacity
for the black-faced spoonbill to a level much lower than that in the
pre-bottleneck era. The deterioration of its wintering habitat is
unlikely to have been responsible for the past bottleneck event because
the habitat has deteriorated continually, which is inconsistent with the
recent population recovery (Baillie, Hilton-Taylor, & Stuart, 2004).
Habitat deterioration would reduce the environmental carrying capacity
of the black-faced spoonbill and constrain the recovery potential and
persistence of this endangered species. Unless stringent conservation
measures are taken to improve or at least maintain its current carrying
capacity, the future of the black-faced spoonbill is still in doubt
despite its recent rapid population growth (Sung, Tse, & Yu, 2018).
Although our results support the conclusion that the black-faced
spoonbill experienced a recent severe population bottleneck, its
genome-wide genetic diversity (π and mean individual
heterozygosity) is comparable to that of the royal spoonbill and other
non-vulnerable avian species (Table S5, S6). This is probably because
the short bottleneck duration and the rapid population recovery only led
to the loss of rare genetic variants. This is what is suggested by the
lower frequency of singleton SNPs in the folded site frequency spectrum
(Fig. 3C) and higher genome-wide Tajima’s D (> 0)
values in the black-faced spoonbill. This observation is consistent with
a simulation study: a short bottleneck is less likely to cause severe
genetic erosion (Allendorf, 1986). Since standing genetic variation with
variants present at high frequencies could allow a species to respond
more swiftly to selection pressures posed by changing environments
(Hermisson & Pennings, 2005; Lande & Shannon, 1996), our results
suggest that the recent drastic population bottleneck event might not
severely dampen the evolutionary potential of the black-faced spoonbill.
Therefore, if its further population recovery can be sustained, the
chance for this once critically endangered wader to cope with future
environmental changes should be approximately the same as for royal
spoonbills and other non-vulnerable species.
Although the extant black-faced spoonbill might not be suffering from
severe genetic erosion, it could still be the victim of an elevated
level of inbreeding (Fig. 3) and mutation load (Fig. 4). However,
despite the fact that these birds carry higher numbers of detrimental
mutations, its population has still grown steadily since 1988 (Yu et
al., 2020). One possible explanation for this is that the fitness effect
of mutations could be environment-dependent (Szafraniec, Borts, &
Korona, 2001): the high genetic load in the black-faced spoonbill might
not necessarily confer lower population fitness in a benign environment.
However, when the environment becomes more stressful, the impact of
mutations’ deleterious effects on fitness could increase (Martin &
Lenormand, 2006), especially when exacerbated anthropogenic
environmental change is expected to further reduce the habitat quality
of wildlife for the foreseeable future. Therefore, even the black-faced
spoonbill population rebound led to its being down-listed from
critically endangered to endangered in the IUCN Red List, and is
considered a success example of international collaborative conservation
efforts (BirdLife International, 2000), our study suggests that these
birds are not totally out of the woods yet.
Furthermore, our results provide an example of modern genomic sequencing
technologies as a powerful tool to monitor the genetic health of and
predict the evolutionary potential for any species whose conservation is
of concern. In the case of black-faced spoonbills, genomic data suggest
that even after decades of rapid population rebound, its fate is still
in the mists and further conversation measures are needed to assure its
survival given that its habitat will inevitably be subject to tremendous
anthropogenic impacts. Given both theoretical (Robertson & Waddington,
1960; Hill & Robertson, 1966) and empirical (Weber, 2004) works
suggesting that selection is more effective in larger populations, rapid
population recovery after a bottleneck event may be critical to restore
the efficacy of selection to purge out accumulated detrimental
mutations. Aiding the re-expansion of the black-faced spoonbill should
be considered as an overarching objective of its conservation management
in near future. All conservation practices, such as habitat restoration
(Dobson, Bradshaw, & Baker, 1997), supplementary feeding (Ewen, Walker,
Canessa, & Groombridge, 2015), predator removal (Smith, Pullin,
Stewart, & Sutherland, 2010), and population augmentation from ex
situ population(Bowkett, 2009) should be seriously considered and
employed. In addition, we propose that the level of inbreeding and
mutation load of black-faced spoonbill individuals should be continually
monitored. Such information would provide temporal genomic indices (such
as ROH) to evaluate how its genetic health has been improved by current
conservation practices to assist its population recovery strategy. Taken
together, our results are especially relevant when anthropogenic
environmental changes are increasingly turning incidental natural
processes into catastrophic events which put many wildlife species in
great peril of population reduction.