Signatures of local adaptation in Embothrium coccineum
One of our objectives was to disentangle the effects of local adaptation
and isolation by environment (IBE) from neutral processes, such as
isolation by distance (IBD) or co-ancestry linked to the species glacial
history (IBA), in shaping among-population genetic differentiation ofE. coccineum . Our results show that the observed pattern of
genetic variation is, at least in part, the result of adaptation to the
strong environmental gradients characterizing the species distribution
range (Danield and Veblen 2000; Souto and Premoli 2007; Souto et al.,
2009; Souto and Smouse, 2013). Indeed, results from the redundancy
analysis (RDA) show that IBE was a significant driver of population
structure and explained the largest amount of among-population variation
in E. coccineum , even after controlling for IBD and IBA. These
results were corroborated by the much higher divergence detected between
the North and Center-South genetic groups in the NJ tree based on
genetic distance calculated using only the outlier loci putatively under
selection than the one observed when using all the loci genotyped.
Our gradient forest analysis identifies precipitation of the driest
month as the most important explanatory environmental variable
explaining E. coccineum pattern of genetic variation. The level
of precipitation of the driest month distinguishes the northern
neighboring Mediterranean biome and the Patagonian steep close to the
east, both with very low summer precipitation, from the temperate biome
inhabited by E. coccineum (Escobar et al., 2006). The second
explanatory environmental variable was the mean temperature of the
wettest quarter. This result is consistent with studies focused on other
Proteaceae; with summer rainfall associated with differences in
functional traits in P. rapens (Carlson et al., 2016) and inProtea section Exsertae (i.e., a group of sixProtea species; Carlson et al., 2011; Prunier et al., 2012,
Prunier et al., 2017). Differences in morphology associated with
environmental gradients have already been reported in E.
coccineum (Chalcof, 2008; Souto and Premoli, 2007), supporting the idea
of possible local adaptation in the species. Access to water seem to be
key in determining the ecotypes observed in each region with individuals
from the northern and driest part of the distribution developing as
short plants, of 0.5-2.5 m in height, with small leaves while the
individuals in wet temperate forest of the center part of the
distribution can reach more than 10 m in height and develop very large
leaves (Souto et al., 2009; Souto and Smouse 2013). Plants in areas
characterized by steady and high rainfall may be on average less heat
and water-stressed, favoring the production of leaves that are larger
and broader and maximizing the photosynthetic area when risks of
overheating and drought stress are low (Givnish, 1987; Hallik et al.,
2009). Indeed, a reduction in leaf size has been proposed as one of the
key traits allowing plants to withstand water deficit (B and Xu, 2007,
Peguero-Pina et al., 2014). For example, a reduction in Quercus
faginea leaf size has been proposed as one of the key traits allowing
Mediterranean oaks to withstand the water deficit characteristic of the
region (Baldocchi and Xu, 2007, Peguero-Pina et al., 2014).
To complement the results of the present study it would be interesting
to investigate in detail the possible genetic adaptations of E.
coccineum to different soil chemical properties. Indeed, the species
cluster roots are highly specialized in phosphor mobilization and uptake
(Delgado et al., 2021) and it has been described that energy allocation
to cluster roots varies between regions with a lower cluster roots
growth in plants from the northern part of the species distribution
(Bertin Benavides et al. 2020; Zuñiga-Feest et al., 2015).