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.