Evidence of local adaptation despite strong drift in a Neotropical patchily distributed bromeliad.

Both genetic drift and divergent selection are predicted to be drivers of population differentiation across patchy habitats, but the extent to which these forces act on natural populations to shape traits is strongly affected by species' ecological features. In this study, we infer the genomic structure of Pitcairnia lanuginosa, a widespread herbaceous perennial plant with a patchy distribution. We sampled populations in the Brazilian Cerrado and the Central Andean Yungas and discovered and genotyped SNP markers using double-digest restriction-site associated DNA sequencing. In addition, we analyzed ecophysiological traits obtained from a common garden experiment and compared patterns of phenotypic and genetic divergence (PST-FST comparisons) in a subset of populations from the Cerrado. Our results from molecular analyses pointed to extremely low genetic diversity and a remarkable population differentiation, supporting a major role of genetic drift. Approximately 0.3% of genotyped SNPs were flagged as differentiation outliers by at least two distinct methods, and Bayesian generalized linear mixed models revealed a signature of isolation by environment in addition to isolation by distance for high-differentiation outlier SNPs among the Cerrado populations. PST-FST comparisons suggested divergent selection on two ecophysiological traits linked to drought tolerance. We showed that these traits vary among populations, although without any particular macro-spatial pattern, suggesting local adaptation to differences in micro-habitats. Our study shows that selection might be a relevant force, particularly for traits involved in drought stress, even for populations experiencing strong drift, which improves our knowledge on eco-evolutionary processes acting on non-continuously distributed species.

Dispersal and local persistence shape the genetic structure of a widespread Neotropical plant species with a patchy distribution.

BACKGROUND AND AIMS: Isolated populations constitute an ideal laboratory to study the consequences of intraspecific divergence, because intrinsic incompatibilities are more likely to accumulate under reduced gene flow. Here, we use a widespread bromeliad with a patchy distribution, Pitcairnia lanuginosa, as a model to infer processes driving Neotropical diversification and, thus, to improve our understanding of the origin and evolutionary dynamics of biodiversity in this highly speciose region. METHODS: We assessed the timing of lineage divergence, genetic structural patterns and historical demography of P. lanuginosa, based on microsatellites, and plastid and nuclear sequence data sets using coalescent analyses and an Approximate Bayesian Computation framework. Additionally, we used species distribution models (SDMs) to independently estimate potential changes in habitat suitability. KEY RESULTS: Despite morphological uniformity, plastid and nuclear DNA data revealed two distinct P. lanuginosa lineages that probably diverged through dispersal from the Cerrado to the Central Andean Yungas, following the final uplift of the Andes, and passed through long-term isolation with no evidence of migration. Microsatellite data indicate low genetic diversity and high levels of inbreeding within populations, and restricted gene flow among populations, which are likely to be a consequence of bottlenecks (or founder events), and high selfing rates promoting population persistence in isolation. SDMs showed a slight expansion of the suitable range for P. lanuginosa lineages during the Last Glacial Maximum, although molecular data revealed a signature of older divergence. Pleistocene climatic oscillations thus seem to have played only a minor role in the diversification of P. lanuginosa, which probably persisted through adverse conditions in riparian forests. CONCLUSIONS: Our results imply drift as a major force shaping the evolution of P. lanuginosa, and suggest that dispersal events have a prominent role in connecting Neotropical open and forest biomes.