Comparative transcriptome analysis reveals lineage- and environment-specific adaptations in cacti from the Brazilian Atlantic Forest.

MAIN CONCLUSION: Natural selection influenced adaptive divergence between Cereus fernambucensis and Cereus insularis, revealing key genes governing abiotic stress responses and supporting neoteny in C. insularis. Uncovering the molecular mechanisms driving adaptive divergence in traits related to habitat adaptation remains a central challenge. In this study, we focused on the cactus clade, which includes Cereus sericifer F.Ritter, Cereus fernambucensis Lem., and Cereus insularis Hemsley. These allopatric species inhabit distinct relatively drier regions within the Brazilian Atlantic Forest, each facing unique abiotic conditions. We leveraged whole transcriptome data and abiotic variables datasets to explore lineage-specific and environment-specific adaptations in these species. Employing comparative phylogenetic methods, we identified genes under positive selection (PSG) and examined their association with non-synonymous genetic variants and abiotic attributes through a PhyloGWAS approach. Our analysis unveiled signatures of selection in all studied lineages, with C. fernambucensis northern populations and C. insularis showing the most PSGs. These PSGs predominantly govern abiotic stress regulation, encompassing heat tolerance, UV stress response, and soil salinity adaptation. Our exclusive observation of gene expression tied to early developmental stages in C. insularis supports the hypothesis of neoteny in this species. We also identified genes associated with abiotic variables in independent lineages, suggesting their role as environmental filters on genetic diversity. Overall, our findings suggest that natural selection played a pivotal role in the geographic range of these species in response to environmental and biogeographic transitions.

A historical stepping-stone path for an island-colonizing cactus across a submerged "bridge" archipelago.

Here we use population genomic data (ddRAD-Seq) and ecological niche modeling to test biogeographic hypotheses for the divergence of the island-endemic cactus species Cereus insularis Hemsl. (Cereeae; Cactaceae) from its sister species C. fernambucensis Lem. The Cereus insularis grows in the Fernando de Noronha Islands (FNI), a Neotropical archipelago located 350 km off the Brazilian Atlantic Forest (BAF) coast. Phylogeographic reconstructions support a northward expansion by the common ancestor of C. insularis and C. fernambucensis along the mainland BAF coast, with C. insularis diverging from the widespread mainland taxon C. fernambucensis after colonizing FNI in the late Pleistocene. The morphologically distinct C. insularis is monophyletic and nested within C. fernambucensis, as expected from a progenitor-derivative speciation model. We tested alternative biogeographic and demographic hypotheses for the colonization of the FNI using Approximate Bayesian Computation. We found the greatest support for a stepping-stone path that emerged during periods of decreased sea level (the "bridge" hypothesis), in congruence with historical ecological niche modeling that shows highly suitable habitats on stepping-stone islands during glacial periods. The outlier analyses reveal signatures of selection in C. insularis, suggesting a putative role of adaptation driving rapid anagenic differentiation of this species in FNI.