Replicated radiations in the South American marsh pitcher plants (Heliamphora) lead to convergent carnivorous trap morphologies.

PREMISE: The evolution of carnivorous pitcher traps across multiple angiosperm lineages represents a classic example of morphological convergence. Nevertheless, no comparative study to-date has examined pitcher evolution from a quantitative morphometric perspective. METHODS: In the present study, we used comparative morphometric approaches to quantify the shape space occupied by Heliamphora pitchers and to trace evolutionary trajectories through this space to examine patterns of divergence and convergence within the genus. We also investigated pitcher development, and, how the packing of pitchers is affected by crowding, a common condition in their natural environments. RESULTS: Our results showed that Heliamphora pitchers have diverged along three main axes in morphospace: (1) pitcher curvature; (2) nectar spoon elaboration; and (3) pitcher stoutness. Both curvature and stoutness are correlated with pitcher size, suggesting structural constraints in pitcher morphological evolution. Among the four traits (curvature, spoon elaboration, stoutness, and size), all but curvature lacked phylogenetic signal and showed marked convergence across the phylogeny. We also observed tighter packing of pitchers in crowded conditions, and this effect was most pronounced in curved, slender pitchers. CONCLUSIONS: Overall, our study demonstrates that diversification and convergent evolution of carnivory-related traits extends to finer evolutionary timescales, reinforcing the notion that ecological specialization may not necessarily be an evolutionary dead end.

A new species of Iochroma Benth. (Solanaceae) from the eastern Andes of Colombia.

Iochromaorozcoae A.Orejuela & S.D.Sm., sp. nov. (Solanaceae) is described from the Andean forests of Cundinamarca in the eastern cordillera of Colombia. Iochromaorozcoae was first collected by the eminent Spanish priest and botanist José Celestino Mutis in the late part of the 18th century, but the specimens have lain unrecognised in herbaria for over 200 years. The species shares many features with its closest relative, Iochromabaumii S.D.Sm. & S.Leiva, but it differs from it in having small flowers with five corolla lobes and few inflorescences per branch, located near the shoot apex with 1 to 4 (-8) flowers, fruits that are greenish-yellow when ripe and its restricted geographic distribution. A description of I.orozcoae is provided, along with a detailed illustration, photographs of live plants, a comparison with closely-related species and a key to all Colombian species of Iochroma Benth. In closing, we emphasise the value of historical collections for the knowledge of biodiversity.

ResumenIochromaorozcoae A.Orejuela & S.D.Sm., sp. nov. (Solanaceae) se describe a partir de los bosques andinos de Cundinamarca, en la cordillera oriental de Colombia. Iochromaorozcoae fue recolectada por primera vez por el eminente sacerdote y botánico español José Celestino Mutis a finales del siglo XVIII, pero los especímenes han permanecido sin ser reconocidos en herbarios durante más de 200 años. La especie comparte muchas características con su pariente más cercano, Iochromabaumii S.D.Sm. & S.Leiva, pero difiere de esta en sus flores más pequeñas con cinco lóbulos de la corola y pocas inflorescencias por rama ubicadas cerca del ápice de la rama, con 1 a 4 (­8) flores por inflorescencia, frutos verde-amarillentos al madurar, y su distribución geográfica restringida. Se presenta una descripción de I.orozcoae, junto con una ilustración detallada, fotografías en vivo, una comparación con las especies cercanamente relacionadas y una clave para las especies colombianas de Iochroma Benth. Finalmente, enfatizamos el valor de las colecciones históricas para el conocimiento de la biodiversidad.

Fossil berries reveal global radiation of the nightshade family by the early Cenozoic.

Fossil discoveries can transform our understanding of plant diversification over time and space. Recently described fossils in many plant families have pushed their known records farther back in time, pointing to alternative scenarios for their origin and spread. Here, we describe two new Eocene fossil berries of the nightshade family (Solanaceae) from the Esmeraldas Formation in Colombia and the Green River Formation in Colorado (USA). The placement of the fossils was assessed using clustering and parsimony analyses based on 10 discrete and five continuous characters, which were also scored in 291 extant taxa. The Colombian fossil grouped with members of the tomatillo subtribe, and the Coloradan fossil aligned with the chili pepper tribe. Along with two previously reported early Eocene fossils from the tomatillo genus, these findings indicate that Solanaceae were distributed at least from southern South America to northwestern North America by the early Eocene. Together with two other recently discovered Eocene berries, these fossils demonstrate that the diverse berry clade and, in turn, the entire nightshade family, is much older and was much more widespread in the past than previously thought.

Phylogeny and biogeography of South American marsh pitcher plant genus Heliamphora (Sarraceniaceae) endemic to the Guiana Highlands.

Heliamphora is a genus of carnivorous pitcher plants endemic to the Guiana Highlands with fragmented distributions. We present a well resolved, time-calibrated, and comprehensive Heliamphora phylogeny estimated using Bayesian inference and maximum likelihood based on nuclear genes (26S, ITS, and PHYC) and secondary calibration. We used stochastic mapping to infer ancestral states of morphological characters and ecological traits. Our ancestral state estimations revealed that the pitcher drainage structures characteristic of the genus transformed from a hole to a slit in single clade, while other features (scape pubescence and hammock-like growth) have been gained and lost multiple times. Habitat was similarly labile in Heliamphora, with multiple transitions from the ancestral highland habitats into the lowlands. Using a Mantel test, we found closely related species tend to be geographically closely distributed. Placing our phylogeny in a historical context, major clades likely emerged through both vicariance and dispersal during the Miocene with more recent diversification driven by vertical displacement during the Pleistocene glacial-interglacial thermal oscillations. Despite the dynamic climatic history experienced by Heliamphora, the temperature changes brought by global warming pose a significant threat, particularly for those species at the highest elevations.

Integrating historical biogeography and environmental niche evolution to understand the geographic distribution of Datureae.

PREMISE: The distributions of plant clades are shaped by abiotic and biotic factors as well as historical aspects such as center of origin. Dispersals between distant areas may lead to niche evolution when lineages are established in new environments. Alternatively, dispersing lineages may exhibit niche conservatism, moving between areas with similar environmental conditions. Here we test these contrasting hypotheses in the Datureae clade (Solanaceae). METHODS: We used maximum likelihood methods to estimate the ancestral range of Datureae along with the history of biogeographic events. We then characterized the niche of each taxon using climatic and soil variables and tested for shifts in environmental niche optima. Finally, we examined how these shifts relate to the niche breadth of taxa and clades within Datureae and the degree of overlap between them. RESULTS: Datureae originated in the Andes and subsequently expanded its range to North America and non-Andean regions of South America. The ancestral niche, and that of most Datura and Trompettia species, is dry, while Brugmansia species likely shifted toward a more mesic environment. Nonetheless, most Datureae present moderate to high overlap in niche breadth today. CONCLUSIONS: The expansion of Datureae into North America was associated with niche conservatism, with dispersal into similarly dry areas as occupied by the ancestral lineage. Subsequent niche evolution, including the apparent shift to a mesic niche in Brugmansia, diversified the range of habitats occupied by species in the tribe Datureae but also led to significant niche overlap among the three genera.

Repeated evolution of a morphological novelty: a phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae).

PREMISE OF THE STUDY: The evolution of novel fruit morphologies has been integral to the success of angiosperms. The inflated fruiting calyx, in which the balloon-like calyx swells to completely surround the fruit, has evolved repeatedly across angiosperms and is postulated to aid in protection and dispersal. We investigated the evolution of this trait in the tomatillos and their allies (Physalideae, Solanaceae). METHODS: The Physalideae phylogeny was estimated using four regions (ITS, LEAFY, trnL-F, waxy) with maximum likelihood (ML) and Bayesian inference. Under the best-fitting ML model of trait evolution, we estimated ancestral states along with the numbers of gains and losses of fruiting calyx accrescence and inflation with Bayesian stochastic mapping. Also, phylogenetic signal in calyx morphology was examined with two metrics (parsimony score and Fritz and Purvis's D). KEY RESULTS: Based on our well-resolved and densely sampled phylogeny, we infer that calyx evolution has proceeded in a stepwise and directional fashion, from non-accrescent to accrescent to inflated. In total, we inferred 24 gains of accrescence, 24 subsequent transitions to a fully inflated calyx, and only two reversals. Despite this lability, fruiting calyx accrescence and inflation showed strong phylogenetic signal. CONCLUSIONS: Our phylogeny greatly improves the resolution of Physalideae and highlights the need for taxonomic work. The comparative analyses reveal that the inflated fruiting calyx has evolved many times and that the trajectory toward this phenotype is generally stepwise and irreversible. These results provide a strong foundation for studying the genetic and developmental mechanisms responsible for the repeated origins of this charismatic fruit trait.

Convergent Evolution at the Pathway Level: Predictable Regulatory Changes during Flower Color Transitions.

The predictability of evolution, or whether lineages repeatedly follow the same evolutionary trajectories during phenotypic convergence remains an open question of evolutionary biology. In this study, we investigate evolutionary convergence at the biochemical pathway level and test the predictability of evolution using floral anthocyanin pigmentation, a trait with a well-understood genetic and regulatory basis. We reconstructed the evolution of floral anthocyanin content across 28 species of the Andean clade Iochrominae (Solanaceae) and investigated how shifts in pigmentation are related to changes in expression of seven key anthocyanin pathway genes. We used phylogenetic multivariate analysis of gene expression to test for phenotypic and developmental convergence at a macroevolutionary scale. Our results show that the four independent losses of the ancestral pigment delphinidin involved convergent losses of expression of the three late pathway genes (F3'5'h, Dfr, and Ans). Transitions between pigment types affecting floral hue (e.g., blue to red) involve changes to the expression of branching genes F3'h and F3'5'h, while the expression levels of early steps of the pathway are strongly conserved in all species. These patterns support the idea that the macroevolution of floral pigmentation follows predictable evolutionary trajectories to reach convergent phenotype space, repeatedly involving regulatory changes. This is likely driven by constraints at the pathway level, such as pleiotropy and regulatory structure.

A new species of Saracha (Solanaceae) from the Central Andes of Peru.

Saracha andina Rob. Fernandez, I. Revilla & E. Pariente, sp. nov. (Solanaceae), a new species endemic to the central Andes of Peru, is described here. The new species differs from other species of Saracha Ruiz & Pav. by the combination of small and coriaceous leaves and clearly tubular flowers. A summary of the taxonomic history of the genus Saracha, an identification key for its species and a phylogenetic analysis of this genus and related genera are provided.

Resumen Saracha andina Rob. Fernandez, I. Revilla & E. Pariente, sp. nov. (Solanaceae), una nueva especie endémica de los Andes centrales del Perú se describe aquí. La nueva especie se distingue de las demás especies de Saracha Ruiz & Pav. por poseer hojas coriáceas pequeñas y flores claramente tubulares. Se proporciona un resumen de la historia taxonómica del género Saracha, una clave de identificación revisada para sus especies y un análisis filogenético del género y géneros afines.

Genetic basis for a rare floral mutant in an Andean species of Solanaceae.

PREMISE OF THE STUDY: White forms of typically pigmented flowers are one of the most common polymorphisms in flowering plants. Although the range of genetic changes that give rise to white phenotypes is well known from model systems, few studies have identified causative mutations in natural populations. METHODS: Here we combine genetic studies, in vitro enzyme assays, and biochemical analyses to identify the mechanism underlying the loss of anthocyanin pigment production in the naturally occurring white-flowered morph of Iochroma calycinum (Solanaceae). KEY RESULTS: Comparison of anthocyanin gene sequences revealed a putative loss-of-function mutation, an 11 amino-acid deletion in dihydroflavonol 4-reductase (DFR), in the white morph. Functional assays of Dfr alleles from blue and white morphs demonstrated that this deletion results in a loss of enzymatic activity, indicating that the deletion could be solely responsible for the lack of pigment production. Consistent with this hypothesis, quantitative PCR showed no significant differences in expression of anthocyanin genes between the morphs. Also, thin layer chromatography confirmed that the white morph continues to accumulate compounds upstream of the DFR enzyme. CONCLUSIONS: Collectively, these experiments indicate that the structural mutation at Dfr underlies the rare white flower morph of I. calycinum. This study is one of only a few examples where a flower color polymorphism is due to a loss-of-function mutation in the coding region of an anthocyanin enzyme. The rarity of such mutations in nature suggests that negative consequences prevent fixation across populations.

Competition for hummingbird pollination shapes flower color variation in Andean solanaceae.

One classic explanation for the remarkable diversity of flower colors across angiosperms involves evolutionary shifts among different types of pollinators with different color preferences. However, the pollinator shift model fails to account for the many examples of color variation within clades that share the same pollination system. An alternate explanation is the competition model, which suggests that color divergence evolves in response to interspecific competition for pollinators, as a means to decrease interspecific pollinator movements. This model predicts color overdispersion within communities relative to null assemblages. Here, we combine morphometric analyses, field surveys, and models of pollinator vision with a species-level phylogeny to test the competition model in the primarily hummingbird-pollinated clade Iochrominae (Solanaceae). Results show that flower color as perceived by pollinators is significantly overdispersed within sites. This pattern is not simply due to phylogenetic history: phylogenetic community structure does not deviate from random expectations, and flower color lacks phylogenetic signal. Moreover, taxa that occur in sympatry occupy a significantly larger volume of color space than those in allopatry, supporting the hypothesis that competition in sympatry drove the evolution of novel colors. We suggest that competition among close relatives may commonly underlie floral divergence, especially in species-rich habitats where congeners frequently co-occur.