Genomic signatures of ecological divergence between savanna and forest populations of a Neotropical tree.

BACKGROUND AND AIMS: In eastern Neotropical South America, the Cerrado, a large savanna vegetation, and the Atlantic Forest harbour high biodiversity levels, and their habitats are rather different from each other. The biomes have intrinsic evolutionary relationships, with high lineage exchange that can be attributed, in part, to a large contact zone between them. The genomic study of ecotypes, i.e. populations adapted to divergent habitats, can be a model to study the genomic signatures of ecological divergence. Here, we investigated two ecotypes of the tree Plathymenia reticulata, one from the Cerrado and the other from the Atlantic Forest, which have a hybrid zone in the ecotonal zone of Atlantic Forest-Cerrado. METHODS: The ecotypes were sampled in the two biomes and their ecotone. The evolutionary history of the divergence of the species was analysed with double-digest restriction site-associated DNA sequencing. The genetic structure and the genotypic composition of the hybrid zone were determined. Genotype-association analyses were performed, and the loci under putative selection and their functions were investigated. KEY RESULTS: High divergence between the two ecotypes was found, and only early-generation hybrids were found in the hybrid zone, suggesting a partial reproductive barrier. Ancient introgression between the Cerrado and Atlantic Forest was not detected. The soil and climate were associated with genetic divergence in Plathymenia ecotypes and outlier loci were found to be associated with the stress response, with stomatal and root development and with reproduction. CONCLUSIONS: The high genomic, ecological and morphophysiological divergence between ecotypes, coupled with partial reproductive isolation, indicate that the ecotypes represent two species and should be managed as different evolutionary lineages. We advise that the forest species should be re-evaluated and restated as vulnerable. Our results provide insights into the genomic mechanisms underlying the diversification of species across savanna and forest habitats and the evolutionary forces acting in the species diversification in the Neotropics.

The protected tree Dimorphandra wilsonii (Fabaceae) is a population of inter-specific hybrids: recommendations for conservation in the Brazilian Cerrado/Atlantic Forest ecotone.

BACKGROUNDS AND AIMS: Dimorphandra wilsonii Rizzini, a critically endangered and protected tree, has a restricted distribution in the ecotone between the Cerrado and the Atlantic Forest in south-eastern Brazil. In this area, it co-occurs with D. mollis Benth., a common tree from the Cerrado, and D. exaltata Schott., a rare tree from the Atlantic Forest. Previous studies of D. wilsonii indicated heterozygosity excess at the individual level. Field observation of some intermediate phenotypes between D. wilsonii and both congeners suggests hybridization of D. wilsonii with D. mollis and/or D. exaltata. Here, we tested the hypothesis that D. wilsonii may have originated from hybridization between D. exaltata and D. mollis. We also performed cytogenetic analysis to examine if the heterozygosity excess could be explained by polyploidy in D. wilsonii. METHODS: We evaluated the genetic diversity and population structure of D. wilsonii using 11 nuclear simple sequence repeats (SSRs) genotyped in 152 individuals sampled across the taxon's range. We performed comparative genetic analyses using overlapping SSR markers between D. wilsonii and previously published SSR data in D. mollis and D. exaltata to subsequently perform a series of allelic comparisons, multivariate and Bayesian analysis. KEY RESULTS: Our results suggest that D. wilsonii individuals are most likely to correspond to F1 hybrids between D. exaltata and D. mollis. Cytogenetic analysis indicated that D. wilsonii is diploid with the same chromosome number as D. mollis (2n = 2x = 28). CONCLUSIONS: Our study raises questions about the taxonomic status and the evolutionary future of D. wilsonii. We suggest that the conservation and management strategy for D. wilsonii should be revised and that it should take into account both parental Dimorphandra species in the ecotone, with special emphasis on the threatened D. exaltata. Finally, this study highlights the value of genetic information for the design of conservation strategies.

Hybrid zone of a tree in a Cerrado/Atlantic Forest ecotone as a hotspot of genetic diversity and conservation.

The Cerrado, the largest Neotropical savanna, and the Brazilian Atlantic Forest form large ecotonal areas where savanna and forest habitats occupy adjacent patches with closely related species occurring side by side, providing opportunities for hybridization. Here, we investigated the evolutionary divergence between the savanna and forest ecotypes of the widely distributed tree Plathymenia reticulata (n = 233 individuals). Genetic structure analysis of P. reticulata was congruent with the recognition of two ecotypes, whose divergence captured the largest proportion of genetic variance in the data (F CT = 0.222 and F ST = 0.307). The ecotonal areas between the Cerrado and the Atlantic Forest constitute a hybrid zone in which a diversity of hybrid classes was observed, most of them corresponding to second-generation hybrids (F2) or backcrosses. Gene flow occurred mainly toward the forest ecotype. The genetic structure was congruent with isolation by environment, and environmental correlates of divergence were identified. The observed pattern of high genetic divergence between ecotypes may reflect an incipient speciation process in P. reticulata. The low genetic diversity of the P. reticulata forest ecotype indicate that it is threatened in areas with high habitat loss on Atlantic Forest. In addition, the high divergence from the savanna ecotype suggests it should be treated as a different unit of management. The high genetic diversity found in the ecotonal hybrid zone supports the view of ecotones as important areas for the origin and conservation of biodiversity in the Neotropics.

Genetic data improve the assessment of the conservation status based only on herbarium records of a Neotropical tree.

Although there is a consensus among conservation biologists about the importance of genetic information, the assessment of extinction risk and conservation decision-making generally do not explicitly consider this type of data. Genetic data can be even more important in species where little other information is available. In this study, we investigated a poorly known legume tree, Dimorphandra exaltata, from the Brazilian Atlantic Forest, a hotspot for conservation. We coupled species distribution models and geospatial assessment based on herbarium records with population genetic analyses to evaluate its genetic status and extinction risk, and to suggest conservation measures. Dimorphandra exaltata shows low genetic diversity, inbreeding, and genetic evidence of decrease in population size, indicating that the species is genetically depleted. Geospatial assessment classified the species as Endangered. Species distribution models projected a decrease in range size in the near future (2050). The genetic status of the species suggests low adaptive potential, which compromises its chances of survival in the face of ongoing climatic change. Altogether, our coupled analyses show that the species is even more threatened than indicated by geospatial analyses alone. Thus, conservation measures that take into account genetic data and the impacts of climate change in the species should be implemented.

Disentangling the Environmental Factors That Shape Genetic and Phenotypic Leaf Trait Variation in the Tree Qualea grandiflora Across the Brazilian Savanna.

Identifying the environmental factors that shape intraspecific genetic and phenotypic diversity of species can provide insights into the processes that generate and maintain divergence in highly diverse biomes such as the savannas of the Neotropics. Here, we sampled Qualea grandiflora, the most widely distributed tree species in the Cerrado, a large Neotropical savanna. We analyzed genetic variation with microsatellite markers in 23 populations (418 individuals) and phenotypic variation of 10 metamer traits (internode, petiole and corresponding leaf lamina) in 36 populations (744 individuals). To evaluate the role of geography, soil, climate, and wind speed in shaping the divergence of genetic and phenotypic traits among populations, we used Generalized Dissimilarity Modelling. We also used multiple regressions to further investigate the contributions of those environmental factors on leaf trait diversity. We found high genetic diversity, which was geographically structured. Geographic distance was the main factor shaping genetic divergence in Qualea grandiflora, reflecting isolation by distance. Genetic structure was more related to past climatic changes than to the current climate. We also found high metamer trait variation, which seemed largely influenced by precipitation, soil bulk density and wind speed during the period of metamer development. The high degree of metamer trait variation seems to be due to both, phenotypic plasticity and local adaptation to different environmental conditions, and may explain the success of the species in occupying all the Cerrado biome.