Gene flow and uneven divergence across the genome
The establishment of reproductive isolation is an important landmark of speciation completion (Feder, Egan, & Nosil, 2012; Wu, 2001; Wu & Ting, 2004). Interbreeding between complete species is impeded by various forms of behavioral, ecological or genetical incompatibilities (Seehausen et al., 2014). Subspecies, on the other hand, are in the middle to late stages of speciation, before the establishment of strong reproductive isolation. This permits gene flow between subspecies wherever hard geographic isolation is absent. In our case, A. m. marina and A. m. eucalyptifolia co-occur on Western Australian coasts. A recent study identified seven genetic clusters of populations along the 2,400 kilometers of these coasts. Although the authors claimed equal possibility to sample individuals from both subspecies, their clustering analyses didn’t reveal subspecies differentiation (Binks et al., 2019). Our data provide direct evidence for the gene flow between subspecies in that location, consistent with observations from the previous study. Moreover, gene flow is not limited to Western Australia, but is common to all three subspecies.
We find that A. marina subspecies have achieved stable morphological and genetic distinctness but not strong reproductive isolation. At this stage, the genome has not yet diverged as a collective unit. Thus, using a few markers randomly selected from the genome is not likely to be sufficient to stably distinguish these varietal groups. Instead, some regions, usually accounting for a small portion of the genome (for example, about 5% of the genome in this study), diverge significantly but the rest of the genome is mixed by gene flow. The highly divergent part of the genome is not necessarily a single block on one chromosome, but is usually sparsely dispersed across the genome. Even though specific genes underlying the divergent phenotypes are not mapped, this genomic pattern of uneven divergence is typical for the subspecies stage.
In conclusion, our deep survey of genetic variation among populations ofA. marina from a wide geographic range and large genomic scope, confirms the designation of three subspecies within A. marina . Subspecies should show features including: (1) distinct morphological traits and higher level of genetic divergence between pairs of populations from different than from the same subspecies; (2) separate demographic history; (3) complete geographical isolation is not mandatory for subspecies and gene flow between them is possible where ranges overlap; (4) Delineation of subspecies varies from locus to locus, suggesting inconsistent genetic divergence across the genome, and hinting continual (and uneven) exchange of genes from locus to locus. These features from a population genetic prospective could be applied to assessment of subspecies in other domain of the tree of life.