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).