Subgenome composition but not ploidy is associated with local
ocean salinity
Studies in other systems indicate that an increase in ploidy tends to be
associated with increased salt tolerance both within and between closely
related species (Chao et al., 2013; Wu et al., 2019; Yang et al., 2014).
However, when ploidy is considered alone, there is no detectable
difference in local ocean salinity between diploid and triploid P.
vaginatum (Fig. 5). Instead, copy number of the P. vaginatumsubgenome may be the driving factor. Gene dosage effects can have a
dramatic influence on phenotypes and increased copy number of salt
tolerance genes has been implicated in the evolution of salt tolerance
in halophytes (Oh, Dassanayake, Bohnert, & Cheeseman, 2012). Variation
in gene copy number can also occur on a whole genome level in
populations of hybrids that vary in the number of subgenomes they
received from each parental species. Other studies have investigated
reciprocal allotriploid hybrids (e.g. 1:2 vs 2:1), similar to those we
describe here, which are often more similar to the parent from which
they received two copies (Betto-Colliard, Hofmann, Sermier, Perrin, &
Stöck, 2018; Harvey, Fjelldal, Solberg, Hansen, & Glover, 2017; Tan et
al., 2016; Yao, Gray, Auger, & Birchler, 2013).
Our results support the hypothesis that the other unknown subgenome
present in the coarse-textured ecotype is not as adapted for saline
environments as is P. vaginatum (Fig 5). Plants with two copies
of the P. vaginatum subgenome (fine-textured, and 2:1 triploids)
were found in locations where the local ocean salinity was on average
~15% higher than those with only one copy (1:1 diploids
and 1:2 triploids). The effect of increasing counts of the unknown
subgenome was weaker and in the opposite direction (slightly less ocean
salinity with each copy). We cannot say for certain whether this weaker
effect is due to increased ploidy or subgenome dosage effects, or both.
If it is a ploidy effect then it is the opposite of predictions that
polyploids should be more salt tolerant.
The large effect of the number of P. vaginatum subgenomes is
consistent with our finding that coarse-textured hybrids are likely
“general-purpose genotypes” because their local ocean salinity is not
only lower, but also more variable. Furthermore, unlike most other
studies of reciprocal triploids, we can rule out maternal subgenome
effects because all of the coarse-textured hybrids carry the same cpDNA
haplotype, implying the same maternal parent species for each cross.
Although the trend we observe between P. vaginatum subgenome copy
number and local salinity is striking, environmental associations are
necessarily correlational in nature and must be confirmed with
controlled salt tolerance assays and transcriptomics. It is also
possible that unknown demographic or introduction history could
contribute to these patterns. Additionally, our sea surface salinity
dataset does not have the resolution to identify the microhabitat
variation likely experienced by plants in the wild (for example, in an
estuary with a steep salinity gradient). While higher resolution
salinity data exist for some coastal areas, temporal and methodological
variation between datasets make them unsuited for comparison across the
geographic scale of this study.