INTRODUCTION
Species is widely considered as the basic entity of biodiversity in
nature, although different species concepts have been proposed and used
(Zachos, 2016). The most popular biological species concept (BSC) uses
reproductive isolation as the gold standard to designate species. In
taxonomy, subspecies is used to denote recognizable infraspecific
differentiation above populations. Conventionally, subspecies is defined
as “a geographically defined aggregate of local populations which
differ taxonomically from other subdivisions of the species” by E. Mayr
(1940, 1963). In the context of BSC, subspecies can interbreed without a
fitness penalty (Patten, 2015), although a test of this ability is
usually not practically possible in the wild. The designation of
subspecies has been criticized as arbitrary and rejected by some
taxonomists (Wilson & Brown, 1953; Hawlitschek, Nagy, & Glaw, 2012;
Phillimore & Owens, 2006; Torstrom, Pangle, & Swanson, 2014).) Others
insist on the value of the subspecies rank (Durrant, 1955; Mayr, 1982;
Phillimore & Owens, 2006), with the emphasis on unique geographic range
or habitat, phylogenetically concordant phenotypic characters, and
unique natural history (O’Brien & Mayr, 1991).
Given the taxa designated as subspecies, conventionally basing on
morphological and geographical evidences, we would expect that the
designation itself represents a level of genetic variation at somewhere
between geographical populations and full species. It requires some
examinations on the pattern of genetic variations, which may strengthen
or weaken the subspecies designation. Many studies have tested whether
defined subspecies are monophyletic on phylogenetic trees constructed
using a handful of genetic markers (Moritz, 1994; Phillimore & Owens,
2006). However, it provides little assessment of the divergence level,
because monophyly is also evidence of full species and the alternative
is normally interpreted as a deficit of divergence. Instead, we propose
that divergence among, given polymorphism within, subspecies should be
assessed using population genetic analyses, since speciation proceeds at
the population level.
The reduction in cost of sequencing allows us to quantify genetic
divergence across the genome in large population samples. With such data
in hand we can ask the following questions: What are the patterns of
genomic variation among taxa a priori designated as subspecies?
Do these patterns strengthen or weaken the subspecies designation? We
start from investigating the taxa that can be reasonably designated as
subspecies by conventional criteria. We perform such a study on the
mangrove tree Avicennia marina . It is the most wide-ranging
mangrove species, reaching the most marginal mangrove patches of the
Indo-West Pacific region (Duke, 2006; Tomlinson, 2016). The taxonomy of
Indo-West Pacific (IWP) Avicennia had been troublesome before
Duke’s comprehensive revision (Duke, 1991). In that assessment, A.
marina were divided into three varieties (Duke, 1991). After that
division, “varieties” or “subspecies” were used to refer to the
three groups by different authors (Duke, 2006; Duke, Benzie, Goodall, &
Ballment, 1998; Maguire, Peakall, Saenger, & Maguire, 2002; Maguire,
Saenger, Baverstock, & Henry, 2000).
The three subspecies show remarkable differences in morphological traits
and geographical distribution (Duke, 1991, 2006). Details of these
differences are described in the following section. A previous study
used allozyme markers to determine genetic divergence among these
subspecies, in which no fixed differentiation among subspecies was
identified and the populations were genetically clustered into two
groups (Duke et al., 1998). However, the reliability of that study is
greatly compromised because they used very few genetic markers. We
sought to obtain a comprehensive determination of genetic divergence
among the three subspecies as well as reconstructing their evolutionary
history through collecting single nucleotide polymorphisms across close
to a hundred genomic loci.
The clarification of genetic divergence among subspecies may encourage
us to treat these subspecies as different conservation units,
particularly in projects such as transplanting and breeding. As the most
widely distributed mangrove tree, this significance is valuable forA. marina . Mangrove species are all a conservation priority
because these species are ecologically important in sheltering coastal
regions from hurricanes, supporting the intertidal ecosystem, and
sequestering carbon, but they are under great threat of global climate
change in combination with more direct human disturbances (Gilman,
Ellison, Duke, & Field, 2008; Guo et al., 2018a).