Incomplete lineage sorting and hybridization underlie tree discordance in Petunia and related genera (Petunieae, Solanaceae).

Despite the overarching history of species divergence, phylogenetic studies often reveal distinct topologies across regions of the genome. The sources of these gene tree discordances are variable, but incomplete lineage sorting (ILS) and hybridization are among those with the most biological importance. Petunia serves as a classic system for studying hybridization in the wild. While field studies suggest that hybridization is frequent, the extent of reticulation within Petunia and its closely related genera has never been examined from a phylogenetic perspective. In this study, we used transcriptomic data from 11 Petunia, 16 Calibrachoa, and 10 Fabiana species to illuminate the relationships between these species and investigate whether hybridization played a significant role in the diversification of the clade. We inferred that gene tree discordance within genera is linked to hybridization events along with high levels of ILS due to their rapid diversification. Moreover, network analyses estimated deeper hybridization events between Petunia and Calibrachoa, genera that have different chromosome numbers. Although these genera cannot hybridize at the present time, ancestral hybridization could have played a role in their parallel radiations, as they share the same habitat and life history.

Macroevolution of the plant-hummingbird pollination system.

Plant-hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant-hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre-dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build-up of both diversities coinciding temporally, and hence suggesting co-diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species-level interaction data in macroevolutionary studies.

Patterns recovered in phylogenomic analysis of Candida auris and close relatives implicate broad environmental flexibility in Candida/Clavispora clade yeasts.

Fungal pathogens commonly originate from benign or non-pathogenic strains living in the natural environment. The recently emerged human pathogen, Candida auris, is one example of a fungus believed to have originated in the environment and recently transitioned into a clinical setting. To date, however, there is limited evidence about the origins of this species in the natural environment and when it began associating with humans. One approach to overcome this gap is to reconstruct phylogenetic relationships between (1) strains isolated from clinical and non-clinical environments and (2) between species known to cause disease in humans and benign environmental saprobes. C. auris belongs to the Candida/Clavispora clade, a diverse group of 45 yeast species including human pathogens and environmental saprobes. We present a phylogenomic analysis of the Candida/Clavispora clade aimed at understanding the ecological breadth and evolutionary relationships between an expanded sample of environmentally and clinically isolated yeasts. To build a robust framework for investigating these relationships, we developed a whole-genome sequence dataset of 108 isolates representing 18 species, including four newly sequenced species and 18 environmentally isolated strains. Our phylogeny, based on 619 orthologous genes, shows environmentally isolated species and strains interspersed with clinically isolated counterparts, suggesting that there have been many transitions between humans and the natural environment in this clade. Our findings highlight the breadth of environments these yeasts inhabit and imply that many clinically isolated yeasts in this clade could just as easily live outside the human body in diverse natural environments and vice versa.

The sequential direct and indirect effects of mountain uplift, climatic niche and floral trait evolution on diversification dynamics in an Andean plant clade.

Why and how organismal lineages radiate is commonly studied through either assessing abiotic factors (biogeography, geomorphological processes, climate) or biotic factors (traits, interactions). Despite increasing awareness that both abiotic and biotic processes may have important joint effects on diversification dynamics, few attempts have been made to quantify the relative importance and timing of these factors, and their potentially interlinked direct and indirect effects, on lineage diversification. We here combine assessments of historical biogeography, geomorphology, climatic niche, vegetative and floral trait evolution to test whether these factors jointly, or in isolation, explain diversification dynamics of a Neotropical plant clade (Merianieae, Melastomataceae). After estimating ancestral areas and the changes in niche and trait disparity over time, we employ Phylogenetic Path Analyses as a synthesis tool to test eleven hypotheses on the individual direct and indirect effects of these factors on diversification rates. We find strongest support for interlinked effects of colonization of the uplifting Andes during the mid-Miocene and rapid abiotic climatic niche evolution in explaining a burst in diversification rate in Merianieae. Within Andean habitats, later increases in floral disparity allowed for the exploitation of wider pollination niches (i.e., shifts from bee to vertebrate pollinators), but did not affect diversification rates. Our approach of including both vegetative and floral trait evolution, rare in assessments of plant diversification in general, highlights that the evolution of woody habit and larger flowers preceded the colonization of the Andes, but was likely critical in enabling the rapid radiation in montane environments. Overall, and in concert with the idea that ecological opportunity is a key element of evolutionary radiations, our results suggest that a combination of rapid niche evolution and trait shifts were critical for the exploitation of newly available niche space in the Andes in the mid-Miocene. Further, our results emphasize the importance of incorporating both abiotic and biotic factors into the same analytical framework if we aim to quantify the relative and interlinked effects of these processes on diversification.

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.

Opposing Patterns of Altitude-Driven Pollinator Turnover in the Tropical and Temperate Americas.

AbstractAbiotic factors (e.g., temperature, precipitation) vary markedly along elevational gradients and differentially affect major groups of pollinators. Ectothermic bees, for example, are impeded in visiting flowers by cold and rainy conditions common at high elevations, while endothermic hummingbirds may continue foraging under such conditions. Despite the possibly far-reaching effects of the abiotic environment on plant-pollinator interactions, we know little about how these factors play out at broad ecogeographic scales. We address this knowledge gap by investigating how pollination systems vary across elevations in 26 plant clades from the Americas. Specifically, we explore Cruden's 1972 hypothesis that the harsh montane environment drives a turnover from insect to vertebrate pollination at higher elevations. We compared the elevational distribution and bioclimatic attributes for a total of 2,232 flowering plants and found that Cruden's hypothesis holds only in the tropics. Above 30°N and below 30°S, plants pollinated by vertebrates (mostly hummingbirds) tend to occur at lower elevations than those pollinated by insects. We hypothesize that this latitudinal transition is due to the distribution of moist, forested habitats favored by vertebrate pollinators, which are common at high elevations in the tropics but not in the temperate Americas.

Evolutionary walks through flower colour space driven by gene expression in Petunia and allies (Petunieae).

The structure and function of biochemical and developmental pathways determine the range of accessible phenotypes, which are the substrate for evolutionary change. Accordingly, we expect that observed phenotypic variation across species is strongly influenced by pathway structure, with different phenotypes arising due to changes in activity along pathway branches. Here, we use flower colour as a model to investigate how the structure of pigment pathways shapes the evolution of phenotypic diversity. We focus on the phenotypically diverse Petunieae clade in the nightshade family, which contains ca 180 species of Petunia and related genera, as a model to understand how flavonoid pathway gene expression maps onto pigment production. We use multivariate comparative methods to estimate co-expression relationships between pathway enzymes and transcriptional regulators, and then assess how expression of these genes relates to the major axes of variation in floral pigmentation. Our results indicate that coordinated shifts in gene expression predict transitions in both total anthocyanin levels and pigment type, which, in turn, incur trade-offs with the production of UV-absorbing flavonol compounds. These findings demonstrate that the intrinsic structure of the flavonoid pathway and its regulatory architecture underlies the accessibility of pigment phenotypes and shapes evolutionary outcomes for floral pigment production.

Comparative genomics and phylogenomic investigation of the class Geoglossomycetes provide insights into ecological specialization and the systematics of Pezizomycotina.

Despite their global presence and ubiquity, members of the class Geoglossomycetes (Pezizomycotina, Ascomycota) are understudied systematically and ecologically. These fungi have long been presumed saprobic due to their occurrence in or near leaf litter and soils. Additionally, they lack an apparent association with other organisms, reinforcing this perception. However, observations of sporocarps near ericaceous shrubs have given rise to an alternative hypothesis that members of Geoglossomycetes may form ericoid mycorrhizae or ectomycorrhizae. This claim, however, has yet to be confirmed via microscopy or amplicon-based studies examining root communities. As a result, our current understanding of their ecology is based on cursory observations. This study presents a comparative analysis of genomic signatures related to ecological niche to investigate the hypothesis of an ericoid mycorrhizal or ectomycorrhizal ecology in the class. We compared the carbohydrate-active enzyme (CAZyme) and secondary metabolite contents of six newly sequenced Geoglossomycetes genomes with those of fungi representing specific ecologies across Pezizomycotina. Our analysis reveals CAZyme and secondary metabolite content patterns consistent with ectomycorrhizal (EcM) members of Pezizomycotina. Specifically, we found a reduction in CAZyme-encoding genes and secondary metabolite clusters that suggests a mutualistic ecology. Our work includes the broadest taxon sampling for a phylogenomic study of Pezizomycotina to date. It represents the first functional genomic and genome-scale phylogenetic study of the class Geoglossomycetes and improves the foundational knowledge of the ecology and evolution of these understudied fungi.

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.

Genome sequence for the blue-flowered Andean shrub Iochroma cyaneum reveals extensive discordance across the berry clade of Solanaceae.

The tomato (Solanum lycopersicum L.) family, Solanaceae, is a model clade for a wide range of applied and basic research questions. Currently, reference-quality genomes are available for over 30 species from seven genera, and these include numerous crops as well as wild species [e.g., Jaltomata sinuosa (Miers) Mione and Nicotiana attenuata Torr. ex S. Watson]. Here we present the genome of the showy-flowered Andean shrub Iochroma cyaneum (Lindl.) M. L. Green, a woody lineage from the tomatillo (Physalis philadelphica Lam.) subfamily Physalideae. The assembled size of the genome (2.7 Gb) is more similar in size to pepper (Capsicum annuum L.) (2.6 Gb) than to other sequenced diploid members of the berry clade of Solanaceae [e.g., potato (Solanum tuberosum L.), tomato, and Jaltomata]. Our assembly recovers 92% of the conserved orthologous set, suggesting a nearly complete genome for this species. Most of the genomic content is repetitive (69%), with Gypsy elements alone accounting for 52% of the genome. Despite the large amount of repetitive content, most of the 12 I. cyaneum chromosomes are highly syntenic with tomato. Bayesian concordance analysis provides strong support for the berry clade, including I. cyaneum, but reveals extensive discordance along the backbone, with placement of chili pepper and Jaltomata being highly variable across gene trees. The I. cyaneum genome contributes to a growing wealth of genomic resources in Solanaceae and underscores the need for expanded sampling of diverse berry genomes to dissect major morphological transitions.

Convergent evolution of disordered lipidic structural colour in the fruits of Lantana strigocamara (syn. L. camara hybrid cultivar).

The majority of plant colours are produced by anthocyanin and carotenoid pigments, but colouration obtained by nanostructured materials (i.e. structural colours) is increasingly reported in plants. Here, we identify a multilayer photonic structure in the fruits of Lantana strigocamara and compare it with a similar structure in Viburnum tinus fruits. We used a combination of transmission electron microscopy (EM), serial EM tomography, scanning force microscopy and optical simulations to characterise the photonic structure in L. strigocamara. We also examine the development of the structure during maturation. We found that the structural colour derives from a disordered, multilayered reflector consisting of lipid droplets of c.105 nm that form a plate-like structure in 3D. This structure begins to form early in development and reflects blue wavelengths of light with increasing intensity over time as the structure develops. The materials used are likely to be lipid polymers. Lantana strigocamara is the second origin of a lipid-based photonic structure, convergently evolved with the structure in Viburnum tinus. Chemical differences between the lipids in L. strigocamara and those of V. tinus suggest a distinct evolutionary trajectory with implications for the signalling function of structural colours in fruits.

How to approach the study of syndromes in macroevolution and ecology.

Syndromes, wherein multiple traits evolve convergently in response to a shared selective driver, form a central concept in ecology and evolution. Recent work has questioned the existence of some classic syndromes, such as pollination and seed dispersal syndromes. Here, we discuss some of the major issues that have afflicted research into syndromes in macroevolution and ecology. First, correlated evolution of traits and hypothesized selective drivers is often relied on as the only evidence for adaptation of those traits to those hypothesized drivers, without supporting evidence. Second, the selective driver is often inferred from a combination of traits without explicit testing. Third, researchers often measure traits that are easy for humans to observe rather than measuring traits that are suited to testing the hypothesis of adaptation. Finally, species are often chosen for study because of their striking phenotypes, which leads to the illusion of syndromes and divergence. We argue that these issues can be avoided by combining studies of trait variation across entire clades or communities with explicit tests of adaptive hypotheses and that taking this approach will lead to a better understanding of syndrome-like evolution and its drivers.

Transcription Factors Evolve Faster Than Their Structural Gene Targets in the Flavonoid Pigment Pathway.

Dissecting the relationship between gene function and substitution rates is key to understanding genome-wide patterns of molecular evolution. Biochemical pathways provide powerful systems for investigating this relationship because the functional role of each gene is often well characterized. Here, we investigate the evolution of the flavonoid pigment pathway in the colorful Petunieae clade of the tomato family (Solanaceae). This pathway is broadly conserved in plants, both in terms of its structural elements and its MYB, basic helix-loop-helix, and WD40 transcriptional regulators, and its function has been extensively studied, particularly in model species of petunia. We built a phylotranscriptomic data set for 69 species of Petunieae to infer patterns of molecular evolution across pathway genes and across lineages. We found that transcription factors exhibit faster rates of molecular evolution (dN/dS) than their targets, with the highly specialized MYB genes evolving fastest. Using the largest comparative data set to date, we recovered little support for the hypothesis that upstream enzymes evolve slower than those occupying more downstream positions, although expression levels do predict molecular evolutionary rates. Although shifts in floral pigmentation were only weakly related to changes affecting coding regions, we found a strong relationship with the presence/absence patterns of MYB transcripts. Intensely pigmented species express all three main MYB anthocyanin activators in petals, whereas pale or white species express few or none. Our findings reinforce the notion that pathway regulators have a dynamic history, involving higher rates of molecular evolution than structural components, along with frequent changes in expression during color transitions.

Intraspecific breakdown of self-incompatibility in Physalis acutifolia (Solanaceae).

Variation in mating systems is prevalent throughout angiosperms, with many transitions between outcrossing and selfing above and below the species level. This study documents a new case of an intraspecific breakdown of self-incompatibility in a wild relative of tomatillo, Physalis acutifolia. We used controlled greenhouse crosses to identify self-incompatible (SI) and self-compatible (SC) individuals grown from seed sampled across seven sites across Arizona and New Mexico. We measured 14 flower and fruit traits to test for trait variation associated with mating system. We also quantified pollen tube growth in vivo and tested for the presence of the S-RNase proteins in SI and SC styles. We found that seed from six of the seven sites produced SI individuals that terminated self-pollen tubes in the style and showed detectable S-RNase expression. By contrast, seed from one Arizona site produced SC individuals with no S-RNase expression. These SC individuals displayed typical selfing-syndrome traits such as smaller corollas, reduced stigma-anther distances, and a smaller pollen-ovule ratio. We also found plasticity in self-incompatibility as most of the SI individuals became SC and lost S-RNase expression roughly after 6 months in the greenhouse. While fixed differences in mating systems are known among the SI wild species and the often SC domesticated tomatillos, our study is the first to demonstrate intraspecific variation in natural populations as well as variation in SI over an individual's lifespan.

Structure and contingency determine mutational hotspots for flower color evolution.

Evolutionary genetic studies have uncovered abundant evidence for genomic hotspots of phenotypic evolution, as well as biased patterns of mutations at those loci. However, the theoretical basis for this concentration of particular types of mutations at particular loci remains largely unexplored. In addition, historical contingency is known to play a major role in evolutionary trajectories, but has not been reconciled with the existence of such hotspots. For example, do the appearance of hotspots and the fixation of different types of mutations at those loci depend on the starting state and/or on the nature and direction of selection? Here, we use a computational approach to examine these questions, focusing the anthocyanin pigmentation pathway, which has been extensively studied in the context of flower color transitions. We investigate two transitions that are common in nature, the transition from blue to purple pigmentation and from purple to red pigmentation. Both sets of simulated transitions occur with a small number of mutations at just four loci and show strikingly similar peaked shapes of evolutionary trajectories, with the mutations of the largest effect occurring early but not first. Nevertheless, the types of mutations (biochemical vs. regulatory) as well as their direction and magnitude are contingent on the particular transition. These simulated color transitions largely mirror findings from natural flower color transitions, which are known to occur via repeated changes at a few hotspot loci. Still, some types of mutations observed in our simulated color evolution are rarely observed in nature, suggesting that pleiotropic effects further limit the trajectories between color phenotypes. Overall, our results indicate that the branching structure of the pathway leads to a predictable concentration of evolutionary change at the hotspot loci, but the types of mutations at these loci and their order is contingent on the evolutionary context.

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.