The evolution of glandularity as a defense against herbivores in the tarweed clade.

PREMISE: Glandular trichomes are implicated in direct and indirect defense of plants. However, the degree to which glandular and non-glandular trichomes have evolved as a consequence of herbivory remains unclear, because their heritability, their association with herbivore resistance, their trade-offs with one another, and their association with other functions are rarely quantified. METHODS: We conducted a phylogenetic comparison of trichomes and herbivore resistance against the generalist caterpillar, Heliothis virescens, among tarweed species (Asteraceae: Madiinae) and a genetic correlation study comparing those same traits among maternal half-sibs of three tarweed species. RESULTS: Within a tarweed species, we found no evidence that herbivore growth rate decreased on tarweed individuals or maternal sib groups with more glandularity or denser trichomes. However, tarweed species with more glandularity and fewer non-glandular trichomes resulted in slower-growing herbivores. Likewise, a trade-off between glandular and non-glandular trichomes was apparent among tarweed species, but not among individuals or sib groups within a species. CONCLUSIONS: Our results suggest that this key herbivore does not select for trichomes as a direct defense in tarweed species. However, trichomes differed substantially among species and likely affect herbivore pressure on those species. Our results demonstrate that trade-offs among plant traits, as well as inference on the function of those traits, can depend on scale.

Evolutionary genomics of oceanic island radiations.

A recurring feature of oceanic archipelagos is the presence of adaptive radiations that generate endemic, species-rich clades that can offer outstanding insight into the links between ecology and evolution. Recent developments in evolutionary genomics have contributed towards solving long-standing questions at this interface. Using a comprehensive literature search, we identify studies spanning 19 oceanic archipelagos and 110 putative adaptive radiations, but find that most of these radiations have not yet been investigated from an evolutionary genomics perspective. Our review reveals different gaps in knowledge related to the lack of implementation of genomic approaches, as well as undersampled taxonomic and geographic areas. Filling those gaps with the required data will help to deepen our understanding of adaptation, speciation, and other evolutionary processes.

Edaphic specialization onto bare, rocky outcrops as a factor in the evolution of desert angiosperms.

Understanding the processes that enable organisms to shift into more arid environments as they emerge is critical for gauging resilience to climate change, yet these forces remain poorly known. In a comprehensive clade-based study, we investigate recent shifts into North American deserts in the rock daisies (tribe Perityleae), a diverse tribe of desert sunflowers (Compositae). We sample rock daisies across two separate contact zones between tropical deciduous forest and desert biomes in western North America and infer a time-calibrated phylogeny based on target capture sequence data. We infer biome shifts using Bayesian inference with paleobiome-informed models and find evidence for seven independent shifts into desert habitats since the onset of aridification in the late Miocene. The earliest shift occurred out of tropical deciduous forests and led to an extensive radiation throughout North American deserts that accounts for the majority of extant desert rock daisies. Estimates of life history and micro-habitat in the rock daisies reveal a correlation between a suffrutescent perennial life history and edaphic endemism onto rocky outcrops, an ecological specialization that evolved prior to establishment and diversification in deserts. That the insular radiation of desert rock daisies stemmed from ancestors preadapted for dry conditions as edaphic endemics in otherwise densely vegetated tropical deciduous forests in northwest Mexico underscores the crucial role of exaptation and dispersal for shifts into arid environments.

Directionally biased habitat shifts and biogeographically informative cytonuclear discordance in the Hawaiian silversword alliance (Compositae).

PREMISE: Expanded phylogenetic analyses of the Hawaiian silversword alliance (Argyroxiphium, Dubautia, Wilkesia; Compositae) were undertaken to assess evolutionary and biogeographic informativeness of cytonuclear discordance and any biases in evolutionary directionality of ecological transitions within this prominent example of adaptive radiation. METHODS: Samples spanning the geographic and ecological distributions of all recognized taxa were included in phylogenetic and biogeographic analyses of nuclear ribosomal DNA (nrDNA) and cpDNA sequences. Bayesian model testing approaches were used to model ecological evolution and the evolution of nuclear chromosomal arrangements while accounting for phylogenetic uncertainty. RESULTS: Cytonuclear discordance detected previously appears to reflect chloroplast capture, at least in part, with nrDNA trees being largely congruent with nuclear chromosomal structural data and fine-scale taxonomy. Comparison of biogeographic histories estimated from the posterior distributions of nrDNA and cpDNA trees, including inferred chloroplast-capture events, provides additional resolution of dispersal history, including a back-dispersal to Maui Nui from Hawai'i. A newly resolved major nrDNA clade of endemic Kaua'i taxa that mostly were described as new-to-science since the 1980s strengthens the earlier hypothesis that diversification on Kaua'i has not waned since the island began to decline in area through subsidence and erosion. Bias in habitat shifts was estimated, with transitions from dry-to-mesic or -wet and from wet-to-mesic or -bog habitats dominating diversification of the silversword alliance from a dry-adapted tarweed ancestor. CONCLUSIONS: The habitat-transition biases estimated here may indicate more limited pathways of ecological evolution than proposed previously for an adaptive radiation involving such major ecological shifts.

Revisiting the hyperdominance of Neotropical tree species under a taxonomic, functional and evolutionary perspective.

Recent studies have leveraged large datasets from plot-inventory networks to report a phenomenon of hyperdominance in Amazonian tree communities, concluding that few species are common and many are rare. However, taxonomic hypotheses may not be consistent across these large plot networks, potentially masking cryptic diversity and threatened rare taxa. In the current study, we have reviewed one of the most abundant putatively hyperdominant taxa, Protium heptaphyllum (Aubl.) Marchand (Burseraceae), long considered to be a taxonomically difficult species complex. Using morphological, genomic, and functional data, we present evidence that P. heptaphyllum sensu lato may represent eight separately evolving lineages, each warranting species status. Most of these lineages are geographically restricted, and few if any of them could be considered hyperdominant on their own. In addition, functional trait data are consistent with the hypothesis that trees from each lineage are adapted to distinct soil and climate conditions. Moreover, some of the newly discovered species are rare, with habitats currently experiencing rapid deforestation. We highlight an urgent need to improve sampling and methods for species discovery in order to avoid oversimplified assumptions regarding diversity and rarity in the tropics and the implications for ecosystem functioning and conservation.

Vascular plant extinction in the continental United States and Canada.

Extinction rates are expected to increase during the Anthropocene. Current extinction rates of plants and many animals remain unknown. We quantified extinctions among the vascular flora of the continental United States and Canada since European settlement. We compiled data on apparently extinct species by querying plant conservation databases, searching the literature, and vetting the resulting list with botanical experts. Because taxonomic opinion varies widely, we developed an index of taxonomic uncertainty (ITU). The ITU ranges from A to F, with A indicating unanimous taxonomic recognition and F indicating taxonomic recognition by only a single author. The ITU allowed us to rigorously evaluate extinction rates. Our data suggest that 51 species and 14 infraspecific taxa, representing 33 families and 49 genera of vascular plants, have become extinct in our study area since European settlement. Seven of these taxa exist in cultivation but are extinct in the wild. Most extinctions occurred in the west, but this outcome may reflect the timing of botanical exploration relative to settlement. Sixty-four percent of extinct plants were single-site endemics, and many occurred outside recognized biodiversity hotspots. Given the paucity of plant surveys in many areas, particularly prior to European settlement, the actual extinction rate of vascular plants is undoubtedly much higher than indicated here.

Extinción de las Plantas Vasculares en Canadá y los Estados Unidos Continentales Resumen Se espera que las tasas de extinción aumenten durante el Antropoceno. Todavía desconocemos las tasas de extinción actuales de las plantas y muchos animales. Cuantificamos las tasas de extinción de la flora vascular de los Estados Unidos Continentales y Canadá a partir del asentamiento de los europeos. Recopilamos datos sobre especies aparentemente extintas mediante la consulta de bases de datos sobre conservación, búsquedas en la literatura y el escrutinio de la lista resultante con botánicos expertos. Ya que la opinión taxonómica varía ampliamente, desarrollamos un índice de incertidumbre taxonómica (ITU). La ITU abarca desde la A hasta la F, en donde la A indica un reconocimiento taxonómico unánime y la F indica el reconocimiento taxonómico por un sólo autor. La ITU nos permitió evaluar rigurosamente las tasas de extinción. Nuestros datos sugieren que 51 especies y 14 taxones infraespecíficos, que en conjunto representan a 33 familias y a 49 géneros de plantas vasculares, se han extinguido en nuestra área de estudio desde el asentamiento de los europeos. Siete de estos taxones existen en cultivos, pero se encuentran extintos en vida libre. La mayoría de las extinciones ocurrieron en la parte oeste del área de estudio, aunque este resultado puede reflejar el momento de la exploración botánica en relación con el asentamiento europeo. El 64% de las plantas extintas eran endémicas de un sitio único y muchas tuvieron presencia fuera de los puntos calientes de biodiversidad. Dada la escasez de los censos botánicos en muchas áreas, particularmente previo al asentamiento europeo, la tasa actual de extinción de las plantas vasculares es sin duda mucho más alta de lo que se indica en este estudio.

Natural selection maintains species despite frequent hybridization in the desert shrub Encelia.

Natural selection is an important driver of genetic and phenotypic differentiation between species. For species in which potential gene flow is high but realized gene flow is low, adaptation via natural selection may be a particularly important force maintaining species. For a recent radiation of New World desert shrubs (Encelia: Asteraceae), we use fine-scale geographic sampling and population genomics to determine patterns of gene flow across two hybrid zones formed between two independent pairs of species with parapatric distributions. After finding evidence for extremely strong selection at both hybrid zones, we use a combination of field experiments, high-resolution imaging, and physiological measurements to determine the ecological basis for selection at one of the hybrid zones. Our results identify multiple ecological mechanisms of selection (drought, salinity, herbivory, and burial) that together are sufficient to maintain species boundaries despite high rates of hybridization. Given that multiple pairs of Encelia species hybridize at ecologically divergent parapatric boundaries, such mechanisms may maintain species boundaries throughout Encelia.

Facets of phylodiversity: evolutionary diversification, divergence and survival as conservation targets.

Biodiversity is often described as having multiple facets, including species richness, functional diversity and phylogenetic diversity. In this paper, we argue that phylogenetic diversity itself has three distinct facets-lineage diversification, character divergence and survival time-that can be quantified using distinct branch length metrics on an evolutionary tree. Each dimension is related to different processes of macroevolution, has different spatial patterns and is tied to distinct goals for conserving biodiversity and protecting its future resilience and evolutionary potential. We compared the landscapes identified as top conservation priorities by each of these three metrics in a conservation gap analysis for California, a world biodiversity hotspot, using herbarium data on the biogeography and evolutionary relationships of more than 5000 native plant species. Our analysis incorporated a novel continuous metric of current land protection status, fine-scale data on landscape intactness and an optimization algorithm used to identify complementary priority sites containing concentrations of taxa that are evolutionarily unique, vulnerable due to small range size and/or poorly protected across their ranges. Top conservation priorities included pockets of coastal and northern California that ranked highly for all three phylodiversity dimensions and for species richness, as well as sites uniquely identified by each metric whose value may depend on whether properties such as genetic divergence, high net diversification or independent survival experience are most desirable in an Anthropocene flora.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Punctuated plastome reduction and host-parasite horizontal gene transfer in the holoparasitic plant genus Aphyllon.

Foundational studies of chloroplast genome (plastome) evolution in parasitic plants have focused on broad trends across large clades, particularly among the Orobanchaceae, a species-rich and ecologically diverse family of root parasites. However, the extent to which such patterns and processes of plastome evolution, such as stepwise gene loss following the complete loss of photosynthesis (shift to holoparasitism), are detectable at shallow evolutionary time scale is largely unknown. We used genome skimming to assemble eight chloroplast genomes representing complete taxonomic sampling of Aphyllon sect. Aphyllon, a small clade within the Orobanchaceae that evolved approximately 6 Ma, long after the origin of holoparasitism. We show substantial plastome reduction occurred in the stem lineage, but subsequent change in plastome size, gene content, and structure has been relatively minimal, albeit detectable. This lends additional fine-grained support to existing models of stepwise plastome reduction in holoparasitic plants. Additionally, we report phylogenetic evidence based on an rbcL gene tree and assembled 60+ kb fragments of the Aphyllon epigalium mitochondrial genome indicating host-to-parasite horizontal gene transfers (hpHGT) of several genes originating from the plastome of an ancient Galium host into the mitochondrial genome of a recent common ancestor of A. epigalium Ecologically, this evidence of hpHGT suggests that the host-parasite associations between Galium and A. epigalium have been stable at least since its subspecies diverged hundreds of thousands of years ago.

Retracing the Hawaiian silversword radiation despite phylogenetic, biogeographic, and paleogeographic uncertainty.

The Hawaiian silversword alliance (Asteraceae) is an iconic adaptive radiation. However, like many island plant lineages, no fossils have been assigned to the clade. As a result, the clade's age and diversification rate are not known precisely, making it difficult to test biogeographic hypotheses about the radiation. In lieu of fossils, paleogeographically structured biogeographic processes may inform species divergence times; for example, an island must first exist for a clade to radiate upon it. We date the silversword clade and test biogeographic hypotheses about its radiation across the Hawaiian Archipelago by modeling interactions between species relationships, molecular evolution, biogeographic scenarios, divergence times, and island origination times using the Bayesian phylogenetic framework, RevBayes. The ancestor of living silverswords most likely colonized the modern Hawaiian Islands once from the mainland approximately 5.1 Ma, with the most recent common ancestor of extant silversword lineages first appearing approximately 3.5 Ma. Applying an event-based test of the progression rule of island biogeography, we found strong evidence that the dispersal process favors old-to-young directionality, but strong evidence for diversification continuing unabated into later phases of island ontogeny, particularly for Kaua'i. This work serves as a general example for how diversification studies benefit from incorporating biogeographic and paleogeographic components.

Spatial phylogenetics of the native California flora.

BACKGROUND: California is a world floristic biodiversity hotspot where the terms neo- and paleo-endemism were first applied. Using spatial phylogenetics, it is now possible to evaluate biodiversity from an evolutionary standpoint, including discovering significant areas of neo- and paleo-endemism, by combining spatial information from museum collections and DNA-based phylogenies. Here we used a distributional dataset of 1.39 million herbarium specimens, a phylogeny of 1083 operational taxonomic units (OTUs) and 9 genes, and a spatial randomization test to identify regions of significant phylogenetic diversity, relative phylogenetic diversity, and phylogenetic endemism (PE), as well as to conduct a categorical analysis of neo- and paleo-endemism (CANAPE). RESULTS: We found (1) extensive phylogenetic clustering in the South Coast Ranges, southern Great Valley, and deserts of California; (2) significant concentrations of short branches in the Mojave and Great Basin Deserts and the South Coast Ranges and long branches in the northern Great Valley, Sierra Nevada foothills, and the northwestern and southwestern parts of the state; (3) significant concentrations of paleo-endemism in Northwestern California, the northern Great Valley, and western Sonoran Desert, and neo-endemism in the White-Inyo Range, northern Mojave Desert, and southern Channel Islands. Multiple analyses were run to observe the effects on significance patterns of using different phylogenetic tree topologies (uncalibrated trees versus time-calibrated ultrametric trees) and using different representations of OTU ranges (herbarium specimen locations versus species distribution models). CONCLUSIONS: These analyses showed that examining the geographic distributions of branch lengths in a statistical framework adds a new dimension to California floristics that, in comparison with climatic data, helps to illuminate causes of endemism. In particular, the concentration of significant PE in more arid regions of California extends previous ideas about aridity as an evolutionary stimulus. The patterns seen are largely robust to phylogenetic uncertainty and time calibration but are sensitive to the use of occurrence data versus modeled ranges, indicating that special attention toward improving geographic distributional data should be top priority in the future for advancing understanding of spatial patterns of biodiversity.

Species richness and endemism in the native flora of California.

PREMISE OF THE STUDY: California's vascular flora is the most diverse and threatened in temperate North America. Previous studies of spatial patterns of Californian plant diversity have been limited by traditional metrics, non-uniform geographic units, and distributional data derived from floristic descriptions for only a subset of species. METHODS: We revisited patterns of sampling intensity, species richness, and relative endemism in California based on equal-area spatial units, the full vascular flora, and specimen-based distributional data. We estimated richness, weighted endemism (inverse range-weighting of species), and corrected weighted endemism (weighted endemism corrected for richness), and performed a randomization test for significantly high endemism. KEY RESULTS: Possible biases in herbarium data do not obscure patterns of high richness and endemism at the spatial resolution studied. High species richness was sometimes associated with significantly high endemism (e.g., Klamath Ranges) but often not. In Stebbins and Major's (1965) main endemism hotspot, Southwestern California, species richness is high across much of the Peninsular and Transverse ranges but significantly high endemism is mostly localized to the Santa Rosa and San Bernardino mountains. In contrast, species richness is low in the Channel Islands, where endemism is significantly high, as also found for much of the Death Valley region. CONCLUSIONS: Measures of taxonomic richness, even with greater weighting of range-restricted taxa, are insufficient for identifying areas of significantly high endemism that warrant conservation attention. Differences between our findings and those in previous studies appear to mostly reflect the source and scale of distributional data, and recent analytical refinements.

Molecular and morphological evidence for recognition of two species within Harpagonella (Amsinckiinae, Boraginaceae).

Recent taxonomic treatments of the genus Harpagonella have included only one lower taxon, Harpagonella palmeri A. Gray. However, a larger-fruited variety of Harpagonella palmeri from Arizona and Sonora was described by I.M. Johnston in 1924. He continued to recognize this taxon - Harpagonella palmeri var. arizonica - in his treatment of the genus in Kearney and Peebles's Arizona Flora in 1960. Here, we provide two lines of molecular evidence and quantitative morphological evidence from calyx characters showing that plants of Harpagonella from Arizona, Sonora, and central Baja California, corresponding to Johnston's var. arizonica, are distinct from Harpagonella palmeri of southern California and Baja California. We make the new combination Harpagonella arizonica (I.M. Johnston) Guilliams & B.G. Baldwin, comb. nov. for the plants from Arizona, Sonora, and central Baja California.

Cryptic host-specific diversity among western hemisphere broomrapes (Orobanche s.l., Orobanchaceae).

BACKGROUND AND AIMS: The broomrapes, Orobanche sensu lato (Orobanchaceae), are common root parasites found across Eurasia, Africa and the Americas. All species native to the western hemisphere, recognized as Orobanche sections Gymnocaulis and Nothaphyllon, form a clade that has a centre of diversity in western North America, but also includes four disjunct species in central and southern South America. The wide ecological distribution coupled with moderate taxonomic diversity make this clade a valuable model system for studying the role, if any, of host-switching in driving the diversification of plant parasites. METHODS: Two spacer regions of ribosomal nuclear DNA (ITS + ETS), three plastid regions and one low-copy nuclear gene were sampled from 163 exemplars of Orobanche from across the native geographic range in order to infer a detailed phylogeny. Together with comprehensive data on the parasites' native host ranges, associations between phylogenetic lineages and host specificity are tested. KEY RESULTS: Within the two currently recognized species of O. sect. Gymnocaulis, seven strongly supported clades were found. While commonly sympatric, members of these clades each had unique host associations. Strong support for cryptic host-specific diversity was also found in sect. Nothaphyllon, while other taxonomic species were well supported. We also find strong evidence for multiple amphitropical dispersals from central North America into South America. CONCLUSIONS: Host-switching is an important driver of diversification in western hemisphere broomrapes, where host specificity has been grossly underestimated. More broadly, host specificity and host-switching probably play fundamental roles in the speciation of parasitic plants.

Pleistocene radiation of the serpentine-adapted genus Hesperolinon and other divergence times in Linaceae (Malpighiales).

PREMISE OF THE STUDY: Hesperolinon (western flax; Linaceae) is endemic to the western United States, where it is notable for its high and geographically concentrated species diversity on serpentine-derived soils and for its use as a model system in disease ecology. We used a phylogenetic framework to test a long-standing hypothesis that Hesperolinon is a neoendemic radiation. METHODS: Five plastid and two ribosomal nuclear DNA gene regions were sampled from 105 populations of Hesperolinon, including all 13 recently recognized species across their known ranges. We used these data to generate population-level phylogenies of Hesperolinon. We also generated a robustly sampled chronogram of Linaceae using an eight-gene, 100-taxon supermatrix calibrated using fossil Linum pollen and a published chronogram of Malpighiales. KEY RESULTS: Most diversification in Hesperolinon has taken place in the past 1-2 million yr, much more recently than previous estimates. Only the earliest-diverging species, H. drymarioides, was resolved as a clade. Denser taxon and gene sampling generally support previously proposed relationships within Linaceae, but with more recent diversification of key clades. CONCLUSIONS: Hesperolinon is an excellent example of edaphic neoendemism, in support of Raven and Axelrod's hypothesis for the genus. Dense population-level sampling reveals a complex of incipient species, with clades poorly aligned with traditional morphological circumscriptions, likely due in part to continued gene flow. The diversification of Linaceae is more recent than previously estimated, and other recent radiations (e.g., Hugonia) warrant further study.

Genetic and ecotypic differentiation in a Californian plant polyploid complex (Grindelia, Asteraceae).

Studies of ecotypic differentiation in the California Floristic Province have contributed greatly to plant evolutionary biology since the pioneering work of Clausen, Keck, and Hiesey. The extent of gene flow and genetic differentiation across interfertile ecotypes that span major habitats in the California Floristic Province is understudied, however, and is important for understanding the prospects for local adaptation to evolve or persist in the face of potential gene flow across populations in different ecological settings. We used microsatellite data to examine local differentiation in one of these lineages, the Pacific Coast polyploid complex of the plant genus Grindelia (Asteraceae). We examined 439 individuals in 10 different populations. The plants grouped broadly into a coastal and an inland set of populations. The coastal group contained plants from salt marshes and coastal bluffs, as well as a population growing in a serpentine grassland close to the coast, while the inland group contained grassland plants. No evidence for hybridization was found at the single location where adjacent populations of the two groups were sampled. In addition to differentiation along ecotypic lines, there was also a strong signal of local differentiation, with the plants grouping strongly by population. The strength of local differentiation is consistent with the extensive morphological variation observed across populations and the history of taxonomic confusion in the group. The Pacific Clade of Grindelia and other young Californian plant groups warrant additional analysis of evolutionary divergence along the steep coast-to-inland climatic gradient, which has been associated with local adaptation and ecotype formation since the classic studies of Clausen, Keck, and Hiesey.

Non-congruent colonizations and diversification in a coevolving pollination mutualism on oceanic islands.

A challenge for coevolutionary theory is how different types of interaction influence the diversification of coevolving clades. Reciprocal specialization is characteristic of certain coevolving, mutualistic interactions, but whether this specialization seen in ecological time constrains changes in patterns of interaction over evolutionary time remains unclear. Here, we examine the co-radiation of Glochidion trees (Phyllanthaceae: Phyllanthus s. l.) and pollinating, seed-predatory Epicephala moths (Lepidoptera: Gracillariidae) on young (mostly later than 5 Ma) oceanic islands in southeastern Polynesia. Epicephala are the sole known pollinators of Glochidion trees, and show extreme reciprocal specialization in continental Asia. We find that Glochidion and Epicephala diversified across these islands through repeated, non-congruent colonizations, and that one recently colonizing Epicephala lineage has spread across 12 host species in three archipelagos in less than 1 Myr. These results indicate that reciprocal specialization and coadaptation do not prevent dramatic changes in associations between intimately associated taxa over short evolutionary time scales. Not only are these host associations more dynamic than previously recognized, but these changes in patterns of interaction may play an important role in the diversification of coevolving taxa.

Floral paedomorphy leads to secondary specialization in pollination of Madagascar Dalechampia (Euphorbiaceae).

The traditional evolutionary interpretation of Von Baer's "laws" of embryology is that retention of early developmental forms into adulthood (paedomorphosis) leads to the evolution of simpler or more generalized morphology and ecology. Here we show that paedomorphosis can also be involved in an increase in ecological specialization, in this case of plant-pollinator relationships. A paedomorphic transition from generalized pollination (by several functional types of pollinators) to specialized pollination (by one or a few species in one functional type) occurred in a clade of endemic Madagascar vines (Dalechampia spp., Euphorbiaceae). This evolutionary transition involved staminate flowers that fail to develop "normally," instead holding mature pollen inside virtually unopened, bud-like flowers. This paedomorphic morphology restricts reward access to "buzz-pollinating" bees, including Xylocopa species (carpenter bees), which can remove pollen by sonication. This is one of very few reports of paedomorphic specialization, and, as far as we are aware, the first documented case of a rapid reversal to specialized pollination in a lineage of plants that had previously switched from specialized to generalized pollination in conjunction with dispersing to a new region.