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.