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Pollinators drive floral evolution in an Atlantic Forest genus

ABSTRACT: Abstract Pollinators are important drivers of angiosperm diversification at both micro- and macroevolutionary scales. Both hummingbirds and bats pollinate the species-rich and morphologically diverse genus Vriesea across its distribution in the Brazilian Atlantic Forest. Here, we (i) determine if floral traits predict functional groups of pollinators as documented, confirming the pollination syndromes in Vriesea and (ii) test if genetic structure in Vriesea is driven by geography (latitudinal and altitudinal heterogeneity) or ecology (pollination syndromes). We analysed 11 floral traits of 58 Vriesea species and performed a literature survey of Vriesea pollination biology. The genealogy of haplotypes was inferred and phylogenetic analyses were performed using chloroplast (rps16-trnk and matK) and nuclear (PHYC) molecular markers. Floral traits accurately predict functional groups of pollinators in Vriesea. Genetic groupings match the different pollination syndromes. Species with intermediate position were found between the groups, which share haplotypes and differ morphologically from the typical hummingbird- and bat-pollinated flowers of Vriesea. The phylogeny revealed moderately to well-supported clades which may be interpreted as species complexes. Our results suggest a role of pollinators driving ecological isolation in Vriesea clades. Incipient speciation and incomplete lineage sorting may explain the overall low genetic divergence within and among morphologically defined species, precluding the identification of clear species boundaries. The intermediate species with mixed floral types likely represent a window into shifts between pollinator syndromes. This study reports the morphological-genetic continuum that may be typical of ongoing pollinator-driven speciation in biodiversity hotspots. In this study, we show floral traits to accurately predict hummingbird and bat pollinators in the Atlantic Forest genus Vriesea. Genetic groupings match the different pollination syndromes. We identify species with intermediate genetic position which differ morphologically from the typical hummingbird- and bat-pollinated Vriesea flowers by their mixed floral traits. We suggest a role of pollinators driving ecological isolation in Vriesea clades and that intermediate species likely represent a window into shifts between pollinators.

SUBMITTER: Neves B

PROVIDER: S-EPMC7532729 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Project description:Aim:Understanding the complex interaction and relative contributions of factors involved in species and trait diversification is crucial to gain insights into the evolution of Neotropical biodiversity. Here, we investigated the drivers of morphological variation in bromeliads along a latitudinal gradient in a biodiversity hotspot. Location:Atlantic Forest, Brazil. Taxon:A species complex in the genus Vriesea (Bromeliaceae). Methods:We measured shape and size variation for 208 floral bracts and 176 leaves in individuals from 14 localities using geometric morphometrics. We compiled data for two chloroplast regions (matK and trnL-F) from 89 individuals to assess genetic diversity, population structure and phylogenetic relationships. We tested the influence of climate, altitude and genetic distance on morphological traits using linear statistical models. Results:Temperature seasonality is a main driver of floral bract shape. Together with precipitation, it also explains changes in leaf size across the latitudinal gradient. Shifts in morphological traits are correlated with genetic structure and partly support the recent taxonomic delimitation proposed for the species complex. The species started to diversify in the Pliocene ca. 5 Mya. We detected a phylogeographical break in species distribution into northern and southern clades between the Bocaina region and the southern portion of the Atlantic Forest. Main Conclusions:We identify how geography and environmental changes through time shape floral bracts and leaves in similar ways. At highly seasonal sites with lower annual precipitation (in the southern subtropical portion of the Atlantic Forest), leaves are larger and floral bracts are wide-elliptic, making them better suited for increased water accumulation. In contrast, at less seasonal sites (in the tropical north, where rainfall is more abundant and temperatures are higher), leaves are narrower and floral bracts are lanceolate-shaped, facilitating water drainage. The biogeographical break we identified suggests a role of tectonic activity and climatic oscillations in promoting species divergence and diversification.

Project description:High-energy freshwater environments such as rapids and waterfalls in the Upper-Paraná Atlantic Forest are home to highly endemic minute freshwater snails of the genus Acrorbis. Only one species, Acrorbis petricola, is currently included within this genus, whose geographical distribution is restricted to three known populations, one in Brazil and the other two in Argentina. Because of habitat specificity and limited geographical distribution, the species is considered vulnerable in Argentina and endangered in Brazil. In this work, we identify five new populations of A. petricola in southern Upper-Paraná Atlantic Forest, exclusively found on waterfalls from the Misiones Province, Argentina. Based on these populations and on specimens of one of the two historical populations from the Misiones Province, we explored the morphological features of shells and reproductive system of specimens from each location and provide the first molecular data on the species. We used DNA sequences from cytochrome c oxidase subunit I (COI) and 16S-rRNA genes to investigate the molecular diversity, genetic distances and genealogical relationships among populations. We verified the existence of intra- and interpopulation morphological variability, with the greatest variation being found in spire, spiral sculpture, penis sheath, flagella, prostatic diverticula and bursa copulatrix. We found interpopulation genetic diversity, with no intrapopulation variation, and identified six geographically structured genetic lineages with maximum genetic distances of up to 2.3%. Different combinations of morphological characters with the same genetic background within each locality were observed. The finding of new populations genetically differentiated not only broadens the known distribution of the species, but also illustrates that waterfall environments in the Atlantic Forest harbour a hidden diversity of Acrorbis that still remains to be discovered. This scenario suggests a complex evolutionary history that needs to be unveiled and taken into account for future development of conservation strategies in this endemic genus.

Project description:Unlabelled•Background and aimsAnimal-pollinated angiosperms have evolved a variety of signalling mechanisms to attract pollinators. Floral scent is a key component of pollinator attraction, and its chemistry modulates both pollinator behaviour and the formation of plant-pollinator networks. The neotropical orchid genus Gongora exhibits specialized pollinator associations with male orchid bees (Euglossini). Male bees visit orchid flowers to collect volatile chemical compounds that they store in hind-leg pouches to use subsequently during courtship display. Hence, Gongora floral scent compounds simultaneously serve as signalling molecules and pollinator rewards. Furthermore, because floral scent acts as the predominant reproductive isolating barrier among lineages, it has been hypothesized that chemical traits are highly species specific. A comparative analysis of intra- and inter-specific variation of floral scent chemistry was conducted to investigate the evolutionary patterns across the genus. •MethodsGas chromatography-mass spectrometry (GC-MS) was used to analyse the floral scent of 78 individuals belonging to 28 different species of Gongora from two of the three major lineages sampled across the neotropical region. Multidimensional scaling and indicator value analyses were implemented to investigate the patterns of chemical diversity within and among taxonomic groups at various geographic scales. Additionally, pollinator observations were conducted on a sympatric community of Gongora orchids exhibiting distinct floral scent phenotypes. •Key resultsA total of 83 floral volatiles, mainly terpenes and aromatic compounds, were detected. Many of the identified compounds are common across diverse angiosperm families (e.g. cineole, eugenol, ?-ocimene, ?-pinene and terpinen-4-ol), while others are relatively rare outside euglossine bee-pollinated orchid lineages. Additionally, 29 volatiles were identified that are known to attract and elicit collection behaviour in male bees. Floral scent traits were less variable within species than between species, and the analysis revealed exceptional levels of cryptic diversity. Gongora species were divided into 15 fragrance groups based on shared compounds. Fragrance groups indicate that floral scent variation is not predicted by taxonomic rank or biogeographic region. •ConclusionsGongora orchids emit a diverse array of scent molecules that are largely species specific, and closely related taxa exhibit qualitatively and quantitatively divergent chemical profiles. It is shown that within a community, Gongora scent chemotypes are correlated with near non-overlapping bee pollinator assemblies. The results lend support to the hypothesis that floral scent traits regulate the architecture of bee pollinator associations. Thus, Gongora provides unique opportunities to examine the interplay between floral traits and pollinator specialization in plant-pollinator mutualisms.

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Pollinators drive floral evolution in an Atlantic Forest genus

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