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.