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).