Replicated radiation of a plant clade along a cloud forest archipelago.

Replicated radiations, in which sets of similar forms evolve repeatedly within different regions, can provide powerful insights into parallel evolution and the assembly of functional diversity within communities. Several cases have been described in animals, but in plants we lack well-documented cases of replicated radiation that combine comprehensive phylogenetic and biogeographic analyses, the delimitation of geographic areas within which a set of 'ecomorphs' evolved independently and the identification of potential underlying mechanisms. Here we document the repeated evolution of a set of leaf ecomorphs in a group of neotropical plants. The Oreinotinus lineage within the angiosperm clade Viburnum spread from Mexico to Argentina through disjunct cloud forest environments. In 9 of 11 areas of endemism, species with similar sets of leaf forms evolved in parallel. We reject gene-flow-mediated evolution of similar leaves and show, instead, that species with disparate leaf forms differ in their climatic niches, supporting ecological adaptation as the driver of parallelism. Our identification of a case of replicated radiation in plants sets the stage for comparative analyses of such phenomena across the tree of life.

Fitness homeostasis across an experimental water gradient predicts species' geographic range and climatic breadth.

Species range sizes and realized niche breadths vary tremendously. Understanding the source of this variation has been a long-term aim in evolutionary ecology and is a major tool in efforts to ameliorate the impacts of changing climates on species distributions. Species ranges that span a large climatic envelope can be achieved by a collection of specialized genotypes locally adapted to a small range of conditions, by genotypes with stable fitness across variable environments, or a combination of these factors. We asked whether fitness expressed along a key niche axis, water availability, could explain a species' realized niche breadth, its geographic range and climate breadth, in 11 species from a clade of jewelflowers whose range sizes vary by two orders of magnitude. Specifically, we explored whether the range size of a species was related to the ability of genotypes (maternal families) to maintain fitness across a range of experimental water availabilities based on 30-year historical field precipitation regimes. We operationally characterized fitness homeostasis through the coefficient of variation in fitness of a genotype (family) across the experimental water gradient. We found that species with genotypes that had high fitness homeostasis, low variation in fitness over our treatments, had larger climatic niche breadth and geographic range in their field distributions. The result was robust to alternate measures of fitness homeostasis. Our results show that the fitness homeostasis of genotypes can be a major factor contributing to niche breadth and range size in this clade. Fitness homeostasis can buffer species from loss of genetic diversity and under changing climates, provides time for adaptation to future conditions.

Genome size evolution is associated with climate seasonality and glucosinolates, but not life history, soil nutrients or range size, across a clade of mustards.

BACKGROUND AND AIMS: We investigate patterns of evolution of genome size across a morphologically and ecologically diverse clade of Brassicaceae, in relation to ecological and life history traits. While numerous hypotheses have been put forward regarding autecological and environmental factors that could favour small vs. large genomes, a challenge in understanding genome size evolution in plants is that many hypothesized selective agents are intercorrelated. METHODS: We contribute genome size estimates for 47 species of Streptanthus Nutt. and close relatives, and take advantage of many data collections for this group to assemble data on climate, life history, soil affinity and composition, geographic range and plant secondary chemistry to identify simultaneous correlates of variation in genome size in an evolutionary framework. We assess models of evolution across clades and use phylogenetically informed analyses as well as model selection and information criteria approaches to identify variables that can best explain genome size variation in this clade. KEY RESULTS: We find differences in genome size and heterogeneity in its rate of evolution across subclades of Streptanthus and close relatives. We show that clade-wide genome size is positively associated with climate seasonality and glucosinolate compounds. Model selection and information criteria approaches identify a best model that includes temperature seasonality and fraction of aliphatic glucosinolates, suggesting a possible role for genome size in climatic adaptation or a role for biotic interactions in shaping the evolution of genome size. We find no evidence supporting hypotheses of life history, range size or soil nutrients as forces shaping genome size in this system. CONCLUSIONS: Our findings suggest climate seasonality and biotic interactions as potential forces shaping the evolution of genome size and highlight the importance of evaluating multiple factors in the context of phylogeny to understand the effect of possible selective agents on genome size.

Convergent evolution in floral morphology in a plant ring species, the Caribbean Euphorbia tithymaloides.

PREMISE: Ring species have long fascinated evolutionary biologists for their potential insights into lineage divergence and speciation across space. Few studies have investigated the potential for convergent or parallel evolution along the diverging fronts of ring species. We investigated a potential case of parallel floral variation in the Caribbean spurge Euphorbia tithymaloides, the only plant system with molecular support as a ring species. The terminal populations of each front, despite being the most divergent, exhibit such similar floral traits that they were originally considered each other's closest relative. METHODS: We evaluated convergence in floral and leaf traits in relation to geography across 95 populations spanning the distribution of E. tithymaloides. We also reanalyzed available genetic data (from previous phylogenetic analyses) in an explicitly spatial framework. RESULTS: Floral morphology appears to have shifted in a convergent fashion along both geographic fronts of E. tithymaloides, resulting in shorter and more compact inflorescences in Antillean populations compared to the typical elongate "slipper-like" cyathia characteristic of the area of origin. Patterns of spatial genetic variation were more consistent with a two-fronted invasion of the Caribbean than with a simpler model of isolation-by-distance. CONCLUSIONS: Floral divergence in E. tithymaloides is consistent with convergent evolution along the two fronts of a ring species. We outline several (not mutually exclusive) mechanisms that could be driving patterns in morphology, including shifts toward generalized pollination with reduced reliance on hummingbirds, shifts in floral structure closely matching available hummingbird bill traits, and shifts toward increased selfing.

The evolution of floral signals in relation to range overlap in a clade of California Jewelflowers (Streptanthus s.l.).

Because of their function as reproductive signals in plants, floral traits experience distinct selective pressures related to their role in speciation, reinforcement, and prolonged coexistence with close relatives. However, few studies have investigated whether population-level processes translate into detectable signatures at the macroevolutionary scale. Here, we ask whether patterns of floral trait evolution and range overlap across a clade of California Jewelflowers reflect processes hypothesized to shape floral signal differentiation at the population level. We found a pattern of divergence in floral scent composition across the clade such that close relatives had highly disparate floral scents given their age. Accounting for range overlap with close relatives explained additional variation in floral scent over time, with sympatric species pairs having diverged more than allopatric species pairs given their age. However, three other floral traits (flower size, scent complexity and flower color) did not fit these patterns, failing to deviate from a null Brownian motion model of evolution. Together, our results suggest that selection for divergence among close relatives in the composition of floral scents may play a key, sustained role in mediating speciation and coexistence dynamics across this group, and that signatures of these dynamics may persist at the macroevolutionary scale.

Use of herbarium data to evaluate weediness in five congeners.

It is often desirable to quantify a plant's relative weediness or synanthropy, that is, the degree to which a species associates with human-caused disturbance, in order to study and understand the biology, ecology and evolution of weeds and invasive plants. Herbarium specimens are among the most accessible and verifiable sources of data on distribution and habitat. However, the habitat distribution of species may not be reflected accurately by herbarium specimen data, due to well-known biases in plant collection. Here, we assess how well herbarium specimens reflect species' weediness, when compared with direct field surveys. We used five species of Melampodium (Asteraceae) and classified their degree of weediness with a modification of Nuorteva's synanthropy index, based on herbarium specimens. We then modelled the distribution of our focal species in Mexico using MaxEnt and identified a polygon of ∼3000 km(2) in the state of Nayarit, Mexico, where there was a high probability of finding all five species. Systematic field searches in the target area documented all visible populations of four species along major and minor roads. Then we, again, classified their degree of weediness with the synanthropy index, based now on field data, and compared. We found that herbarium data were an accurate predictor of a species' weediness relative to its congeners despite the well-documented skew of herbarium data towards natural areas, which our data reflected as well. So, herbarium data can be used to classify species' weediness relative to each other, but not in absolute terms, if the specimens were correctly identified and none of the species were subject to particular collection bias. This study is the first attempt to compare herbarium and field data on this subject and may be relevant for other types of investigations based on herbarium data. Our work also highlights the usefulness of distribution models based on herbarium specimens.

Macroevolutionary patterns of glucosinolate defense and tests of defense-escalation and resource availability hypotheses.

We explored macroevolutionary patterns of plant chemical defense in Streptanthus (Brassicaceae), tested for evolutionary escalation of defense, as predicted by Ehrlich and Raven's plant-herbivore coevolutionary arms-race hypothesis, and tested whether species inhabiting low-resource or harsh environments invest more in defense, as predicted by the resource availability hypothesis (RAH). We conducted phylogenetically explicit analyses using glucosinolate profiles, soil nutrient analyses, and microhabitat bareness estimates across 30 species of Streptanthus inhabiting varied environments and soils. We found weak to moderate phylogenetic signal in glucosinolate classes and no signal in total glucosinolate production; a trend toward evolutionary de-escalation in the numbers and diversity of glucosinolates, accompanied by an evolutionary increase in the proportion of aliphatic glucosinolates; some support for the RAH relative to soil macronutrients, but not relative to serpentine soil use; and that the number of glucosinolates increases with microhabitat bareness, which is associated with increased herbivory and drought. Weak phylogenetic signal in chemical defense has been observed in other plant systems. A more holistic approach incorporating other forms of defense might be necessary to confidently reject escalation of defense. That defense increases with microhabitat bareness supports the hypothesis that habitat bareness is an underappreciated selective force on plants in harsh environments.

Occupation of bare habitats, an evolutionary precursor to soil specialization in plants.

Plant soil specialists contribute greatly to global diversity; however, the ecoevolutionary forces responsible for generating this diversity are poorly understood. We integrate molecular phylogenies with descriptive and experimental ecological data, creating a powerful framework with which to elucidate forces driving soil specialization. Hypotheses explaining edaphic specialization have historically focused on costs of adaptation to elements (e.g., nickel, calcium/magnesium) and accompanying tradeoffs in competitive ability in benign soils. We combine in situ microhabitat data for 37 streptanthoid species (Brassicaceae), soil analyses, and competition experiments with their phylogeny to reconstruct selective forces generating serpentine soil endemism, which has four to five independent origins in this group. Coupling ancestral state reconstruction with phylogenetic independent contrasts, we examine the magnitude and timing of changes in soil and habitat attributes relative to inferred shifts to serpentine. We find large changes in soil chemistry at nodes associated with soil shifts, suggesting that elemental changes occurred concomitantly with soil transitions. In contrast, the amount of bare ground surrounding plants in the field ("bareness"), which is greater in serpentine environments, is conserved across soil-type shifts. Thus, occupation of bare environments preceded shifts to serpentine, and may serve as an evolutionary precursor to harsh elemental soils and environments. In greenhouse experiments, taxa from barer environments are poorer competitors, a tradeoff that may contribute to soil endemism. The hypothesis of occupation of bare habitats as a precursor of soil specialization can be tested in other systems with a similar integrative ecophylogenetic approach, thereby providing deeper insights into this rich source of biodiversity.

Nowhere to run, nowhere to hide: the importance of enemies and apparency in adaptation to harsh soil environments.

Bare, simplified searching environments, often associated with sparsely vegetated harsh soils, may cause both plant and animal inhabitants to be apparent and conspicuous. "Apparency" has been a key concept to explain the diversity of plant defensive chemistry but has been difficult to test. In animals, there is extensive work on camouflage and crypsis, adaptations to apparency that reduce detection by predators. Here, we explore apparency as a challenge in bare soil habitats characterized by sparse vegetative cover for both plants and animals. Using experiment and observation, we show that attack rates from enemies on vulnerable plants and undefended caterpillar models are greater in barer serpentine habitats than in adjacent more vegetated ones. Palatable Streptanthus species (Brassicaceae) may have adapted to apparency with a crypsis defense, typically considered the purview of animals. In Streptanthus breweri, leaf color is locally matched to soil outcrop color, and experimental mismatching of leaf and substrate color increases damage to plants, suggesting adaptation to apparency per se. Herbivore coloration may, too, have been influenced by greater enemy pressure and apparency in these sites. Adaptation to increased enemy pressure and apparency, with concomitant trade-offs in competitive ability, may be an underappreciated aspect of specialization to harsh soils, especially in plants. Apparency may be a useful framework for understanding trade-offs driving soil specialization and global biodiversity patterns.

Single-copy nuclear gene primers for Streptanthus and other Brassicaceae from genomic scans, published data, and ESTs.

PREMISE OF THE STUDY: We report 11 primer sets for nine single-copy nuclear genes in Streptanthus and other Thelypodieae (Brassicaceae) and their utility at tribal-level and species-level phylogenetics in this poorly resolved group. • METHODS AND RESULTS: We selected regions based on a cross-referenced matrix of previous studies and public Brassica expressed sequence tags. To design primers, we used alignments of low-depth-coverage Illumina sequencing of genomic DNA for two species of Brassica mapped onto Arabidopsis thaliana. We report several primer combinations for five regions that consistently amplified a single band and yielded high-quality sequences for at least 70% of the species assayed, and for four additional regions whose utility might be clade specific. • CONCLUSIONS: Our primers will be useful in improving resolution at shallow depths across the Thelypodieae, and likely in other Brassicaceae.

The Caribbean slipper spurge Euphorbia tithymaloides: the first example of a ring species in plants.

A ring species arises when a parental population expands around an area of unsuitable habitat in such a way that when the two fronts meet they behave as distinct species while still being connected through a series of intergrading populations. Ring species offer great possibilities for studying the forces causing species divergence (e.g. the nature of pre-zygotic or post-zygotic reproductive isolation) or helping to maintain species integrity (e.g. reinforcement). Yet, ring species are extremely rare, and have only been documented convincingly in animals. Here, we present phylogenetic analyses of two nuclear gene regions from the Caribbean slipper spurge (Euphorbia tithymaloides) species complex that provide evidence that this group forms a ring species. These data show that the species complex originated in the area where Mexico and Guatemala meet, and expanded around the Caribbean basin along two distinct fronts: one eastward through the Yucatan Peninsula and into the Greater Antilles (GA); one southeastward through northern South America and then northward to the Lesser Antilles and eastern GA. The two terminal forms co-occur in the Virgin Islands and appear to be morphologically and ecologically distinct. Thus, our results suggest that Euphorbia tithymaloides is the first compelling example of a ring species in plants.

Is LEAFY a useful marker gene for the flower-inflorescence boundary in the Euphorbia cyathium?

The flower-like reproductive structure of Euphorbia s.l. (Euphorbiaceae) is widely believed to have evolved from an inflorescence, and is therefore interpreted as a special type of pseudanthium, termed a cyathium. However, fuzzy morphological boundaries between the inflorescence, individual flowers, and organs have fuelled the suggestion that the cyathium does not merely superficially resemble a flower but could actually share developmental genetic pathways with a conventional flower. To test this hypothesis, immunolocalizations of FLORICAULA/LEAFY (LFY), a protein associated with floral identity in many angiosperm species, were performed in developing cyathia of different species of Euphorbia. Expression of the LFY protein was found not only in individual floral primordia (as predicted from results in the model organisms Arabidopsis and Anthirrhinum), but also in the cyathium primordium and in the primordia of partial male inflorescences. These results provide further evidence that the evolution of floral traits in pseudanthial inflorescences often involves expression of floral development genes in the inflorescence apex. This finding blurs the conventional rigid distinction between flowers and inflorescences.

Are spurred cyathia a key innovation? Molecular systematics and trait evolution in the slipper spurges (Pedilanthus clade: Euphorbia, Euphorbiaceae).

The study of traits that play a key role in promoting diversification is central to evolutionary biology. Floral nectar spurs are among the few plant traits that correlate with an enhanced rate of diversification, supporting the claim that they are key innovations. Slight changes in spur morphology could confer some degree of premating isolation, explaining why clades with spurs tend to include more species than their spurless close relatives. We explored whether the cyathial nectar spur of the Pedilanthus clade (Euphorbia) may also function as a key innovation. We estimated the phylogeny of the Pedilanthus clade using one plastid (matK) and three nuclear regions (ITS and two G3pdh loci) and used our results and a Yule model of diversification to test the hypothesis that the cyathial spur correlates with an increased diversification rate. We found a lack of statistical support for the key innovation hypothesis unless specific assumptions regarding the phylogeny apply. However, the young age (hence small size) of the group may limit our ability to detect a significant increase in diversification rate. Additionally, our results confirm previous species designations, indicate higher homoplasy in cyathial than in vegetative features, and suggest a possible Central American origin of the group.

Extinction threat in the Pedilanthus clade (Euphorbia, Euphorbiaceae), with special reference to the recently rediscovered E. conzattii (P. pulchellus).

The type locality of the slipper spurge Euphorbia conzattii has been in doubt because the 1917 type is a mixed collection with vague label data. In recent field work, the species was found on Cerro Espino, Pochutla District, Oaxaca, Mexico. We used the Method for Evaluation of Risk of Extinction for Mexican Wild Species (MER), required to protect a species under Mexican law, to assess the conservation status of E. conzattii and found it to be endangered. We discuss the mixture in the type of this species with E. calcarata and present an updated description and an illustration of E. conzattii. Preliminary MER assessments of the other Mexican Pedilanthus clade species show two species to be extinct (E. cyri, E. dressleri) and four threatened (including E. colligata, E. finkii, E. tehuacana). The remaining eight have more favorable outlooks. We comment on MER robustness and aspects vulnerable to confusion and offer clarifications. Extinction risk is not distributed evenly throughout the clade, with a subclade of leafy treelets from a variety of habitats having the greatest number of endangered species. Extinction risk is distributed across all Pedilanthus-clade habitats; the strongest association noted is that both species from moist highlands are endangered.