Molecular responses to freshwater limitation in the mangrove tree Avicennia germinans (Acanthaceae)

Abstract

Environmental variation along the geographical space can shape populations by natural selection. In the context of global warming and changing precipitation regimes, it is crucial to understand the role of environmental heterogeneity in tropical trees adaptation, given their disproportional contribution to water and carbon biogeochemical cycles. Here, we investigated how heterogeneity in freshwater availability along tropical wetlands has influenced molecular variations of the black mangrove (Avicennia germinans). A total of 57 trees were sampled at seven sites differing markedly in precipitation regime and riverine freshwater inputs. Using 2,297 genome‐wide single nucleotide polymorphic markers, we found signatures of natural selection by the association between variations in allele frequencies and environmental variables, including the precipitation of the warmest quarter and the annual precipitation. Additionally, we found candidate loci for selection based on statistical deviations from neutral expectations of interpopulation differentiation. Most candidate loci within transcribed sequences were functionally associated with central aspects of drought tolerance or plant response to drought. Moreover, our results suggest the occurrence of the rapid evolution of a population, probably in response to sudden and persistent limitations in plant access to soil water, following a road construction in 1974. Observations supporting rapid evolution included the reduction in tree size and changes in allele frequencies and in transcript expression associated with increased drought tolerance through the accumulation of osmoprotectants and antioxidants, biosynthesis of cuticles, protection against protein degradation, stomatal closure, photorespiration and photosynthesis. We describe a major role of spatial heterogeneity in freshwater availability in the specialization of this typically tropical tree.

Geographical and environmental contributions to genomic divergence in mangrove forests

“…IBD, IBB and IBE 6 models. Considering the genetic structure inferred in previous studies (Cruz et al, , 2020Mori et al, 2015) and the environmental heterogeneity throughout the species distribution, we expect that IBB and IBE will be the main models underlying the geographical distance for both species. Finally, after identifying the factors influencing the distributions of the genetic diversity for A. schaueriana and A. germinans, we discuss the implications for conservation and provide suggestions to improve the long-term resilience of the two black mangrove species.…”

“…Sample populations of A. schaueriana and A. germinans are indicated by two capital letters, as shown in Figure 1. germinans, respectively (Cruz et al, , 2020. Sampling locations, which are indicated by two letters, are displayed as described in Table 1.…”

“…In this region, Avicennia is represented mainly by two of the three New World Avicennia species, namely, Avicennia 5 germinans (L.) L. and Avicennia schaueriana Stapf & Leechman ex Moldenke (Schaeffer-Novelli et al, 1990;Duke, 1991). These species present a partly sympatric distribution on the South American coast, where they share a remarkable north-south pattern of genetic divergence, as revealed by selectively neutral microsatellites (Mori et al, 2015) and single nucleotide polymorphisms (SNPs) (Cruz et al, , 2020. A similar pattern of putatively neutral genetic diversity has also been observed in other coastal species, such as Rhizophora mangle (Pil et al, 2011;Francisco et al, 2018) and the mangrove-associated tree Hibiscus pernambucensis (Takayama et al, 2008).…”

“…We performed correlations for the set of all populations and also for the set of samples located northerly from the SEC and for the set of samples located southerly from the SEC because substantial variations in the genetic structure have been reported at smaller geographical scales in mangroves located in these regions (Cruz et al, , 2020Mori et al, 2015). Previous findings indicate that genetic diversity is organized in well-defined groups at the regional scale for both species and even between individuals of A. germinans that are separated by only a few kilometres (Cruz et al, 2020).…”

Sahara mustard as a major threat to desert biodiversity in the southwest United States and the need to integrate contemporary methods to understand its biology

“…Given that our sampling approach was continuous and we expected high selfing rates within subpopulations (Winkler et al, 2019), we deemed H S the more appropriate metric for calculating F IS in this study. Thus, it is inappropriate to calculate F IS values as in table 2 of Phillip.This method has been used to explore a diversity of population-level phenomena and processes in many biological systems(e.g., van Boheemen et al, 2017;Cruz et al, 2020;Villate et al, 2010). Recent studies that use this metric have been published in Ecology and Evolution.…”