An evolutionary disruption of the buzz pollination syndrome in neotropical montane plants.

PREMISE: Under pollinator limitations, specialized pollination syndromes may evolve toward contrasting responses: a generalized syndrome with increased pollinator attraction, pollinator reward, and pollen transfer capacity; or the selfing syndrome with increased self-pollen deposition, but reduced pollinator attraction and pollen transfer capacity. The buzz-pollination syndrome is specialized to explore female vibrating bees as pollinators. However, vibrating bees become less-active pollinators at montane areas of the Atlantic Forest (AF) domain. This study investigated whether the specialized buzz-pollination syndrome would evolve toward an alternative floral syndrome in montane areas of the AF domain, considering a generalized and the selfing syndromes as alternative responses. METHODS: We utilized a lineage within the buzz-pollinated Miconia as study system, contrasting floral traits between montane AF-endemic and non-endemic species. We measured and validated floral traits that were proxies for pollinator attraction, reward access, pollen transfer capacity, and self-pollen deposition. We inferred the evolution of floral trait via phylogenetic comparative methods. RESULTS: AF-endemic species have selectively evolved greater reward access and more frequently had generalist pollination. Nonetheless, AF-endemic species also have selectively evolved toward lower pollen transfer capacity and greater self pollination. These patterns indicated a complex evolutionary process that has jointly favored a generalized and the selfing syndromes. CONCLUSIONS: The buzz pollination syndrome can undergo an evolutionary disruption in montane areas of the AF domain. This floral syndrome is likely more labile than often assumed, allowing buzz-pollinated plants to reproduce in environments where vibrating bees are less-reliable pollinators.

The evolution of ecological specialization underlies plant endemism in the Atlantic Forest.

BACKGROUND AND AIMS: The evolution of ecological specialization is favoured under divergent selection imposed by increased environmental heterogeneity, although specialization can limit the geographical range of organisms, thus promoting endemism. The Atlantic Forest (AF) is an ancient montane domain with high plant endemism, containing different environments for plant specialization. Miconia is the most diverse genus of woody flowering plant within the AF domain, including AF-endemic and non-endemic lineages. We hypothesized that Miconia species have faced increased environmental heterogeneity and consequently have been selected towards increased specialization in the AF domain, and this increased specialization has greatly reduced species geographical ranges, ultimately promoting endemism. Hence, we made the following predictions: (1) AF-endemic species should face greater environmental heterogeneity than non-endemic species; (2) AF-endemic species should be more specialized than non-endemic species; (3) specialization should lead to smaller geographical ranges; (4) specialization and small geographical ranges among AF-endemic species should conform to a selection-driven evolutionary scenario rather than to a neutral evolutionary scenario; and (5) small geographical ranges among AF-endemic species should date back to the occupation of the AF domain rather than to more recent time periods. METHODS: We used geographical, environmental and phylogenetic data on a major Miconia clade including AF-endemic and non-endemic species. We calculated Rao's Q to estimate the environmental heterogeneity faced by species. We used georeferenced occurrences to estimate the geographical ranges of species. We applied environmental niche modelling to infer species niche breadth. We inferred the most likely evolutionary scenario for species geographical range and niche breadth via a model-fitting approach. We used ancestral reconstructions to evaluate species geographical range throughout time. KEY RESULTS: Atlantic Forest-endemic species faced 33-60 % more environmental heterogeneity, with the increase being associated with montane landscapes in the AF. The AF-endemic species were 60 % more specialized overall, specifically over highly variable environmental gradients in AF montane landscapes. Specialization strongly predicted small geographical ranges among AF-endemic species and was a major range-limiting factor among endemic lineages. The AF-endemic species have evolved towards specialization and small geographical ranges under a selection-driven regime, probably imposed by the great environmental heterogeneity in AF montane landscapes. The AF-endemic species underwent a major reduction of geographical range immediately after their evolution, indicating a long-standing effect of selective pressures in the AF domain. CONCLUSION: Environmental heterogeneity imposes selective pressures favouring ecological specialization and small geographical ranges among plant lineages in the AF domain. This selection-driven process has probably promoted plant endemism in the AF domain throughout its history.

Beneath a hairy problem: Phylogeny, morphology, and biogeography circumscribe the new Miconia supersection Discolores (Melastomataceae: Miconieae).

Miconia is among the largest plant genera in the Neotropics and a taxonomically complex lineage. Indeed, molecular phylogenetic data shows that none of its traditionally accepted sections are monophyletic, preventing taxonomic advances within the genus. Miconia is the largest plant genus in the Brazilian Atlantic Forest, including three main lineages, the Leandra s.s. clade (ca. 215 spp.), the Miconia sect. Chaenanthera (24 spp.), and the Miconia discolor clade (estimated 77 spp.). Out of these lineages, the Miconia discolor clade is the only currently lacking phylogenetic data, complicating its taxonomy. In this study, we reconstruct the phylogeny of the Miconia discolor clade, using three plastid (atpF-H, psbK-I, and psaI-accD) and two nuclear (ETS and ITS) markers. We sampled 60 out of the 77 species of the group, representing 78% of its diversity. Taxa were selected considering their distribution, morphology, and previous phylogenetic knowledge. We used the newly reconstructed phylogeny to better understand phylogenetic relationships among Atlantic Forest species and morphologically similar taxa, and to propose a new infrageneric classification for the Miconia discolor clade: the Miconia supersection Discolores. We further studied the evolution of seven morphological characters using a Maximum Likelihood approach, and estimated the ancestral range distribution of various lineages in order to understand the biogeographic history of this clade. We found that dichasial inflorescences represent the ancestral condition within Miconia, subsequently giving rise to scorpioid and glomerulate inflorescences in the studied group. We describe Miconia supersect. Discolores, originated in the Amazon region, which is recognized by a dense layer of branched tricomes covering young branches and non-dichasial inflorescences, including three main lineages: (i) Miconia sect. Albicantes, characterized by persistent bracts and arachnoid indument on the abaxial surface of leaves, mainly distributed in the Amazon basin; (ii) Miconia sect. Discolores, characterized by caducous calyx lobes and glomerulate inflorescences, centered in the Atlantic Forest; and (iii) Miconia sect. Multispicatae, characterized by leaves not completely covered with indument, and capitate stigma, mainly distributed in the Atlantic Forest. All three sections and the supersection originated in the Neogene, between the Late Miocene and the Early Pliocene.