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. K E Y W O R D SAvicennia germinans (Black Mangrove), drought-tolerance, ecological genomics, nextRAD, RNA-Seq, tropical tree | 345 CRUZ et al.

Geographical and environmental contributions to genomic divergence in mangrove forests

“…Conversely, for A. germinans, genetic variation with evidence of selection was correlated with variations in atmospheric temperature patterns, precipitation regimes, solar radiation and tidal amplitude cycles (Table 2). These results corroborate the findings reported by Cruz et al (2020), who performed a functional characterization of putative loci under selection and suggested that differential precipitation regimes play a fundamental role in genetic divergence between populations of this species. Additionally, our findings support the results reported by Bajay et al (2018), who found different profiles of gene expression among populations of Rhizophora mangle located at contrasting latitudes of the Brazilian coast, with differentially expressed genes putatively involved in the responses to variations in temperature, solar radiation, precipitation and flood frequency.…”

“…SNP loci with evidence of natural selection were identified previously by Cruz et al ( , 2020. For A. schaueriana, 86 loci showed considerable deviations from neutral expectations of interpopulation divergence.…”

“…Biological materials were collected and SNP markers were identified as described in previous studies by for A. schaueriana and Cruz et al (2020) for A. germinans.…”

“…In this region, Avicennia is mainly represented by two of the three New World Avicennia species, namely, Avicennia germinans and Avicennia schaueriana (Schaeffer-Novelli et al, 1990;Duke, 1991). These species present a partially 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).…”

“…In addition to neutral processes that shape the diversity of Avicennia species in this region, recent studies have identified various genomic regions possibly associated with adaptive processes relevant to the environmental context of mangroves (Cruz et al, , 2020). These variations have been attributed to climatic and oceanographic factors that vary widely along the latitudinal gradient of the species distribution.…”