Introduction
To what range a species can distribute and how its intraspecific genetic
variations are structured are fundamentally determined by geographical
and ecological factors (Melville & Burchett, 2002). Various forms of
geographical barriers, on the one hand, constrain the margins of a
species’ distribution ranges and, on the other hand, cause abrupt
discontinuities within the range (Hartl & Clark, 1997). To the coastal
plants that disperse propagules by seawater, the geographical barriers
are usually landmasses, open oceans (Thornhill, Mahon, Norenburg, &
Halanych, 2008), and ocean currents. Moreover, limitations of dispersal
ability may further shape their populations, following a pattern called
isolation by distance (IBD), which assumes that the level of
differentiation is positively correlated with geographic distance.
The geographic landscape and ecological landscape are not persistent
throughout history, making the populations of organisms highly dynamic.
Geological actions had changed the geographical landscape gradually in a
macroevolutionary timescale, such as the uplift of the Qinghai-Tibetan
Plateau (Ramstein, Fluteau, Besse, & Joussaume, 1997; Zhisheng,
Kutzbach, Prell, & Porter, 2001) and the closure of the Central America
isthmus (Lessios, 2008). In a smaller timescale, the historic climate
changes, e.g. the Quaternary glaciers, had reshaped the Earth
continuously. For coastal plants, the historic sea-level changes due to
climate changes had caused geographic barriers to emerge and vanish
repeatedly. The emergence of a barrier may subdivide populations while
the vanish of a barrier may reunite diverging populations (Ge et al.,
2015). Hence, the population structure within a species is an integrated
output of the forces dividing populations and those mixing populations.
Other than isolating and connecting populations, historic geographical
and climatic changes also shaped the demographic size of populations.
Typically, the populations of a species contract to refugia or even
become extinct when geographic or ecological conditions are too hostile
to survive (Foufopoulos, Kilpatrick, & Ives, 2011; Hallam & Wignall,
1999; Jackson, Winston, & Coates, 1985; Ozawa, 2010; Paulay, 1990), and
recover and expand when the conditions are ameliorated. During these
processes of “shrinkage-expansion” (i.e., bottleneck), even when the
species survive, a reduction in intraspecific diversity is common
(Haanes, Røed, Flagstad, & Rosef, 2010; Mamuris, Stoumboudi, Stamatis,
Barbieri, & Moutou, 2005; Moum & Árnason, 2001; Tsuchida, Kudô, &
Ishiguro, 2014). In addition to reducing intraspecific diversity, how
would such a bottleneck process influence the population structure
within a species? During the “shrinkage-expansion” process, the
refugial population usually sampled only a small subset of the total
ancestral polymorphisms, and the small population is more likely to lose
inherent polymorphisms and fix new mutations due to intensified genetic
drift and relaxed purifying selection. Moreover, the contracted
population is usually less likely to exchange genes with other
populations due to enhanced isolation. Hence, we hypothesized the
bottleneck process is highly potential in generating novel genetic
structures within species.
Several previous studies have referred to this issue indirectly. In a
coral reef fish, the strong nonequilibrium genetic structure was shown
to be generated by genetic bottlenecks/founder effects associated with
population reduction/extinctions and asymmetric migration or
recolonization (Bay, Caley, & Crozier, 2008). Repeated bottleneck
events during colonization of the parasite Geomydoecus aurie have
been shown to impart genetic structure of a population due to allele
surfing (Demastes, Hafner, Hafner, Light, & Spradling, 2019). The
fine-scale genetic structure of Rhizophora racemosa in the
Cameroon estuary complex was attributed to contemporary processes such
as restricted propagule dispersal, bottleneck events, and recolonization
by founders from ancient local refugia (Ngeve, Van der Stocken,
Menemenlis, Koedam, & Triest, 2017). Despite the awareness that
bottleneck may generate genetic structure, the hypothesis needs to be
comprehensively and explicitly addressed.
The model with which to test this hypothesis should live in a highly
dynamic habitat and be sensitive to habitat change. Mangrove plants, a
group of typical coastal plants, are therefore an ideal model. Mangrove
plants are distributed linearly along coasts and strictly inhabit
tropical and subtropical intertidal zones. In the Quaternary cycles of
glacial and interglacial conditions, climate changes drove the sea level
to change in cycles (Miller et al., 2005; Zachos, Pagani, Sloan, Thomas,
& Billups, 2001). The coastlines shifted following sea-level rise and
drop, and mangrove forests were forced to advance and retreat repeatedly
(Woodroffe & Grindrod, 1991). Hence, we tested the above hypothesis in
mangrove plants, but the underlying reasonability may be general in
other taxa.
Several studies had determined the genetic structure of different
mangrove species, with periodic geographical barriers frequently
identified in places such as the Malay Peninsula and the Wallacea region
(W. Guo et al., 2018; Z. Guo et al., 2016; J. Li et al., 2016; Urashi,
Teshima, Minobe, Koizumi, & Inomata, 2013; Y. Yang et al., 2016, 2017),
in addition to a set of permanent barriers (Duke, 2017). As the historic
sea-level changes eroded barriers periodically, populations of mangrove
species were isolated or connected by intermittent gene flow, which was
previously employed to illustrate the observed population structure
(divergence and admixture) of many coastal species (Banerjee et al.,
2020, 2021; Z. Guo, Guo, et al., 2018; Z. Guo et al., 2016; Westberg &
Kadereit, 2009). Such intermittent gene flow was demonstrated to have
promoted the speciation of mangrove species via a
“mixing-isolation-mixing” mechanism (Z. He et al., 2019). However,
it’s unclear how demographic size changes driven by sea-level changes
have shaped population structure, although some studies have also
reported that bottleneck events were involved in some mangrove species’
demographic histories and caused population diversity reductions (W. Guo
et al., 2020, 2018; Zhou et al., 2010). It’s intriguing to test the
hypothesis that bottleneck events could promote population subdivision.
We performed such a study in the typical mangrove plant Aegiceras
corniculatum , which is always a frontier species in mangrove forests.
Aegiceras corniculatum is distributed widely from India across
Southeast Asia and South China to Australia and west Pacific islands
(Duke, 2014), likely facilitated by its long-distance dispersal via
buoyant propagules. Ge and Sun et al. had used inter-simple sequence
repeat markers to reveal between-population differentiation in the
populations of A. corniculatum in China (Ge & Sun, 1999). Deng
et al. had used amplified fragment length polymorphism markers to reveal
genetic divergences among populations in China, Malay Peninsula, and Sri
Lanka (Deng et al., 2009). However, the genetic pattern of its whole
distribution range remains unaddressed. We sampled 18 populations,
covering the distribution range of A. corniculatum , and used both
Sanger and Illumina Solexa sequencing to obtain single nucleotide
polymorphism (SNP) markers, with which we could ascertain the population
structure of A. corniculatum across its distribution range. Due
to the dominant role of Sundaland and Wallacea barrier in coastal plants
in the IWP, we expected to see the populations of A. corniculatumfrom the Indian Ocean, Southeast Asia (including South China), and
Australasia is exclusively grouped. Moreover, we expected the historic
sea-level changes had shaped demographic size changes of A.
corniculatum populations, particularly, bottleneck event in history is
expectable. Particular interest was devoted to whether bottleneck events
had played a role in generating additional population structure not
attributed to geographic barriers. The findings will deepen our
understanding of population evolution in dynamic geographic and climate
changes and guide efforts to conserve genetic diversity below the
species level.