INTRODUCTION
Taxonomic rank below species has been controversial. E. Mayr (1940,
1963) defined subspecies as “a geographically defined aggregate of
local populations which differ taxonomically from other subdivisions of
the species.” Although critiques had challenged this subspecies
classification and some taxonomists refuse to describe subspecies
(Wilson & Brown, 1953), the value and utility of the subspecies rank
was appreciated by others (Durrant, 1955; Mayr, 1982; Phillimore &
Owens, 2006). By definition, subspecies is now used to identify
populations distinct mainly in three aspects: isolated geographic range
or habitat, phylogenetically concordant phenotypic characters, and
separate history (O’Brien & Mayr, 1991).
Cases where morphological and genotype-based designations disagree have
proven to be particularly challenging (Hawlitschek, Nagy, & Glaw, 2012;
Phillimore & Owens, 2006; Torstrom, Pangle, & Swanson, 2014).
Morphologically defined taxa are often paraphyletic in phylogenetic
analyses (Moritz, 1994; Phillimore & Owens, 2006). Methods
incorporating multiple lines of evidence, including morphological,
genetic and ecological, have been proposed to resolve this impasse
(Patten, 2015).
The current definition of subspecies by Mayr emphasized that speciation
mostly occurs in allopatry. However, the conventional BSC view that the
genome evolves as a single cohesive unit has been challenged (Wu, 2001;
Wu & Ting, 2004; Feder, Egan, & Nosil, 2012; Feder, Flaxman, Egan,
Comeault, & Nosil, 2013; Foote, 2018; Jiggins, 2019). An increasing
number of cases indicate that speciation occurs with gene flow and
without geographical isolation (Brandvain, Kenney, Flagel, Coop, &
Sweigart, 2014; Clarkson et al., 2014; Harr, 2006; Poelstra et al.,
2014; Wang, He, Shi, & Wu, 2020).
In this vein, some authors proposed to modify the definition of
subspecies to “heritable geographic variation in phenotype.” (Patten,
2015; Patten & Remsen, 2017) This implies there is a gene or a set of
genes determining phenotypic variation between subspecies. In other
words, the test of monophyly on the phylogenetic tree constructed by
several molecular markers and several specimens may not be fully
reliable.
Here we investigated the genetic architecture of three varietal groups
of the mangrove tree Avicennia marina to assess when and whether
populations within a species have attained a sufficient level of genetic
divergence to be recognized as subspecies. Notably, in previous
literature, the three groups were referred to as varieties or subspecies
by different authors (Duke, 2006; Duke, Benzie, Goodall, & Ballment,
1998; Maguire, Peakall, Saenger, & Maguire, 2002; Maguire, Saenger,
Baverstock, & Henry, 2000). Although botanists might have used
different terms such as “subspecies”, “varieties” or “forms”,
these assignments are conceptually consistent (Mallet, 2007).
Inhabiting the intertidal zones of tropical and subtropical coasts,Avicennia marina is an ideal model for addressing the genetic
nature of subspecies because its linear distribution makes it much
easier to ascertain the range of its three varietal groups and their
contact regions. A. marina reaches the most marginal regions of
the Indo-West Pacific (IWP), due to its outstanding tolerance to
salinity, drought and temperature (Tomlinson, 2016). Three putative
subspecies have been identified, namely A. m. marina, A. m.
eucalyptifolia and A. m. australasica . There are reports that
these three groups are genetically disjunct but no fixed divergence was
found among them (Duke, 1991, 2017; Duke et al., 1998). The distinction
between populations and subspecies is of particular significance in the
conservation efforts since mangroves are under the threat of climate
change, in combination with more direct human disturbances(Gilman,
Ellison, Duke, & Field, 2008; Z. Guo et al., 2018).