Introduction
Human activities are driving up to one million species to extinction(IPBES, 2019; Pimm et al., 2014). All threatened species are characterized by small population sizes and a declining population trend or have been through population bottlenecks. Theories suggest that when a population becomes small or has gone through a population bottleneck, the drastically augmented random fluctuation of allele frequencies over time (genetic drift) could lead to the loss of its genetic variation, i.e. genetic erosion. This would compromise a species’ potential to evolve in response to the ever-changing environment(Barrett & Schluter, 2008; Lai et al., 2019; Lande & Shannon, 1996; Bijlsma & Loeschcke, 2012), and lower the efficacy of purifying selection in removing deleterious genetic variants(Kimura, 1962; Kirkpatrick & Jarne, 2000) resulting in the accumulation of deleterious mutations in it (mutation load(Kimura, 1962; Kimura, Maruyama, & Crow, 1963). It can also elevate levels of inbreeding that increase homozygosity and the expression of deleterious recessive alleles, thereby reducing individual fitness (Charlesworth & Charlesworth, 1987; Keller & Waller, 2002). Moreover, theories suggest that such detrimental consequences may persist even after a population re-expands (Kirkpatrick & Jarne, 2000). Therefore, further conservation measures would be required to assure the persistence of a re-expanded endangered population. Although a low level of genetic variation and accumulated deleterious mutations were found in endangered or bottlenecked populations (Robinson et al., 2016; Grossen, Guillaume, Keller, & Croll, 2020), results of some genomic studies suggest otherwise: bottlenecked non-African human populations do not have lower genetic variation, and the effectiveness of purifying selection to remove deleterious mutations is not compromised in the European population (Do et al., 2015; Fu, Gittelman, Bamshad, & Akey, 2014; Lohmueller, 2014; Simons, Turchin, Pritchard, & Sella, 2014). This implies that further conservation provisions might not be essential for the long-term survival of a bottlenecked population. Therefore, the ability of a threatened species to persist may partly depend on the extent to which the historical bottleneck event caused a decay in its genetic diversity and an increase in its mutation load.
The once critically endangered migratory wader, the black-faced spoonbill (Platalea minor )(BirdLife International, 2017), could serve as an ideal system to assess the genetic legacy of a bottleneck event in a re-expanding population. P minor winters in the coastal salty wetland habitats of the East Asian coast (Fig. 1A). Its extant breeding colonies are mainly located on uninhabited rocky islets along the western and eastern coast of the Korean Bay (Chong, Pak, Rim, & Kim, 1996; Ding, Lei, Yin, & Liu, 1999; Ueta et al., 2002), and recently expanded to the coast along the Northern Sea of the Japan Basin (Litvinenko & Shibaev, 2005; Shibaev, 2010). This species was described as ‘common’ in documents pre-dating the 1950s (La Touche, 1931; Austin, 1948). However, only 288 individuals were counted within its entire range in 1988 (Kennerley, 1990). Since then, its population size has increased remarkably to 4,864 individuals according to a census in the winter of 2020 (Yu, Li, Tse, & Fong, 2020). A study of mitochondrial diversity suggested that the spoonbill had recently experienced a severe bottleneck (Yeung, Yao, Hsu, Wang, & Li, 2006). However, without a documented history of the timing, magnitude and duration of the bottleneck, we cannot rule out the possibility that its low population size in the 1980s was part of a natural response to the drastic climate changes since the end of the last glacial maximum (LGM), as in some other endangered species (Mays et al., 2018).
To infer the timing and duration of its presumed recent bottleneck event, we first sequenced and obtained a draft assembly of the black-faced spoonbill genome, then re-sequenced the whole-genome of multiple individuals collected from its two major wintering sites in Taiwan and Hong Kong (Yu et al., 2020) (Fig. 1A). We evaluated the extent of genetic diversity and deleterious mutations accumulated in the extant black-faced spoonbill population by comparing its population genomic data to that of its sister species the royal spoonbill (P. regia ) from which it diverged approximately half a million years ago ( Yeung et al., 2011). The royal spoonbill is commonly found in the wetlands of Australia and nearby islands (Fig. 1A), and its conservation status is in the ‘least concern’ category; it does not have a documented history of bottlenecks (Matheu & del Hoyo, 1992). We specifically addressed the following for the black-faced spoonbill: (1) whether the drastic climate change since the end of the LGM significantly impacted its population trajectory before the presumed recent population bottleneck; (2) what the start time, duration and magnitude of the presumed recent bottleneck were; (3) whether the recent bottleneck event, if any, has led to a relaxation of selection and a higher level of inbreeding, genetic drift and the accumulation of deleterious mutations than in the royal spoonbill.