A phylogeny of the evening primrose family (Onagraceae) using a target enrichment approach with 303 nuclear loci.

BACKGROUND: The evening primrose family (Onagraceae) includes 664 species (803 taxa) with a center of diversity in the Americas, especially western North America. Ongoing research in Onagraceae includes exploring striking variation in floral morphology, scent composition, and breeding system, as well as the role of these traits in driving diversity among plants and their interacting pollinators and herbivores. However, these efforts are limited by the lack of a comprehensive, well-resolved phylogeny. Previous phylogenetic studies based on a few loci strongly support the monophyly of the family and the sister relationship of the two largest tribes but fail to resolve several key relationships. RESULTS: We used a target enrichment approach to reconstruct the phylogeny of Onagraceae using 303 highly conserved, low-copy nuclear loci. We present a phylogeny for Onagraceae with 169 individuals representing 152 taxa sampled across the family, including extensive sampling within the largest tribe, Onagreae. Deep splits within the family are strongly supported, whereas relationships among closely related genera and species are characterized by extensive conflict among individual gene trees. CONCLUSIONS: This phylogenetic resource will augment current research projects focused throughout the family in genomics, ecology, coevolutionary dynamics, biogeography, and the evolution of characters driving diversification in the family.

Target Enrichment and Extensive Population Sampling Help Untangle the Recent, Rapid Radiation of Oenothera Sect. Calylophus.

Oenothera sect. Calylophus is a North American group of 13 recognized taxa in the evening primrose family (Onagraceae) with an evolutionary history that may include independent origins of bee pollination, edaphic endemism, and permanent translocation heterozygosity. Like other groups that radiated relatively recently and rapidly, taxon boundaries within Oenothera sect. Calylophus have remained challenging to circumscribe. In this study, we used target enrichment, flanking noncoding regions, gene tree/species tree methods, tests for gene flow modified for target-enrichment data, and morphometric analysis to reconstruct phylogenetic hypotheses, evaluate current taxon circumscriptions, and examine character evolution in Oenothera sect. Calylophus. Because sect. Calylophus comprises a clade with a relatively restricted geographic range, we were able to extensively sample across the range of geographic, edaphic, and morphological diversity in the group. We found that the combination of exons and flanking noncoding regions led to improved support for species relationships. We reconstructed potential hybrid origins of some accessions and note that if processes such as hybridization are not taken into account, the number of inferred evolutionary transitions may be artificially inflated. We recovered strong evidence for multiple evolutionary origins of bee pollination from ancestral hawkmoth pollination, edaphic specialization on gypsum, and permanent translocation heterozygosity. This study applies newly emerging techniques alongside dense infraspecific sampling and morphological analyses to effectively reconstruct the recalcitrant history of a rapid radiation. [Gypsum endemism; Oenothera sect. Calylophus; Onagraceae; phylogenomics; pollinator shift; recent radiation; target enrichment.].

Field bands of marching locust juveniles show carbohydrate, not protein, limitation.

Locusts are grasshoppers that migrate en masse and devastate food security, yet little is known about the nutritional needs of marching bands in nature. While it has been hypothesized that protein limitation promotes locust marching behavior, migration is fueled by dietary carbohydrates. We studied South American Locust (Schistocerca cancellata) bands at eight sites across Argentina, Bolivia, and Paraguay. Bands ate most frequently from dishes containing carbohydrate artificial diets and minimally from balanced, protein, or control (vitamins and salts) dishes-indicating carbohydrate hunger. This hunger for carbohydrates is likely explained by the observation that local vegetation was generally protein-biased relative to locusts' preferred protein to carbohydrate ratio. This study highlights the importance of studying the nutritional ecology of animals in their environment and suggests that carbohydrate limitation may be a common pattern for migrating insect herbivores.

Nutrient supply and accessibility in plants: effect of protein and carbohydrates on Australian plague locust (Chortoicetes terminifera) preference and performance.

In contrast to predictions from nitrogen limitation theory, recent studies have shown that herbivorous migratory insects tend to be carbohydrate (not protein) limited, likely due to increased energy demands, leading them to preferentially feed on high carbohydrate plants. However, additional factors such as mechanical and chemical defenses can also influence host plant choice and nutrient accessibility. In this study, we investigated the effects of plant protein and carbohydrate availability on plant selection and performance for a migratory generalist herbivore, the Australian plague locust, Chortoicetes terminifera. We manipulated the protein and carbohydrate content of seedling wheat (Triticum aestivum L.) by increasing the protein:carbohydrate ratio using nitrogen (N) fertilizer, and manipulated the physical structure of the plants by grinding and breaking down cell walls after drying the plants. Using a full factorial design, we ran both choice and no-choice experiments to measure preference and performance. We confirmed locust preference for plants with a lower protein-carbohydrate ratio (unfertilized plants). Unlike previous studies with mature wild grass species, we found that intact plants supported better performance than dried and ground plants, suggesting that cell wall removal may only improve performance for tougher or more carbohydrate-rich plants. These results add to the growing body of evidence suggesting that several migratory herbivorous species perform better on plants with a lower protein:carbohydrate ratio.

Differential gene expression associated with a floral scent polymorphism in the evening primrose Oenothera harringtonii (Onagraceae).

BACKGROUND: Plant volatiles play an important role in both plant-pollinator and plant-herbivore interactions. Intraspecific polymorphisms in volatile production are ubiquitous, but studies that explore underlying differential gene expression are rare. Oenothera harringtonii populations are polymorphic in floral emission of the monoterpene (R)-(-)-linalool; some plants emit (R)-(-)-linalool (linalool+ plants) while others do not (linalool- plants). However, the genes associated with differential production of this floral volatile in Oenothera are unknown. We used RNA-Seq to broadly characterize differential gene expression involved in (R)-(-)-linalool biosynthesis. To identify genes that may be associated with the polymorphism for this trait, we used RNA-Seq to compare gene expression in six different Oenothera harringtonii tissues from each of three linalool+ and linalool- plants. RESULTS: Three clusters of differentially expressed genes were enriched for terpene synthase activity: two were characterized by tissue-specific upregulation and one by upregulation only in plants with flowers that produce (R)-(-)-linalool. A molecular phylogeny of all terpene synthases identified two putative (R)-(-)-linalool synthase transcripts in Oenothera harringtonii, a single allele of which is found exclusively in linalool+ plants. CONCLUSIONS: By using a naturally occurring polymorphism and comparing different tissues, we were able to identify candidate genes putatively involved in the biosynthesis of (R)-(-)-linalool. Expression of these genes in linalool- plants, while low, suggests a regulatory polymorphism, rather than a population-specific loss-of-function allele. Additional terpene biosynthesis-related genes that are up-regulated in plants that emit (R)-(-)-linalool may be associated with herbivore defense, suggesting a potential economy of scale between plant reproduction and defense.

What do tropical cryptogams reveal? Strong genetic structure in Amazonian bryophytes.

Lowland tropical bryophytes have been perceived as excellent dispersers. In such groups, the inverse isolation hypothesis proposes that spatial genetic structure is erased beyond the limits of short-distance dispersal. Here, we determine the influence of environmental variation and geographic barriers on the spatial genetic structure of a widely dispersed and phylogenetically independent sample of Amazonian bryophytes. Single nucleotide polymorphism data were produced from a restriction site-associated DNA sequencing protocol for 10 species and analyzed through F-statistics and Mantel tests. Neither isolation-by-environment nor the impact of geographic barriers were recovered from the analyses. However, significant isolation-by-distance patterns were observed for 8 out of the 10 investigated species beyond the scale of short-distance dispersal (> 1 km), offering evidence contrary to the inverse isolation hypothesis. Despite a cadre of life-history traits and distributional patterns suggesting that tropical bryophytes are highly vagile, our analyses reveal spatial genetic structures comparable to those documented for angiosperms, whose diaspores are orders of magnitude larger. Dispersal limitation for tropical bryophytes flies in the face of traditional assumptions regarding their dispersal potential, and suggests that the plight of this component of cryptic biodiversity is more dire than previously considered in light of accelerated forest fragmentation in the Amazon.

Phylogeny, host use, and diversification in the moth family Momphidae (Lepidoptera: Gelechioidea).

Insect herbivores and their hostplants constitute much of Earth's described biological diversity, but how these often-specialized associations diversify is not fully understood. We combined detailed hostplant data and comparative phylogenetic analyses of the lepidopteran family Momphidae to explore how shifts in the use of hostplant resources, not just hostplant taxon, contribute to the diversification of a phytophagous insect lineage. We inferred two phylogenetic hypotheses emphasizing relationships among species in the nominate genus, Mompha Hübner. A six-gene phylogeny was constructed with reared exemplars and collections from hostplants in the family Onagraceae from western and southwestern USA, and a cytochrome c oxidase subunit 1 (COI) phylogeny was inferred from collections and publicly available accessions in the Barcode of Life Data System. Species delimitation analyses combined with morphological data revealed ca. 56 undescribed species-level taxa, many of which are hostplant specialists on Onagraceae in the southwestern USA. Our phylogenetic reconstructions divided Momphidae into six major clades: 1) an Onagraceae flower- and fruit-boring clade, 2) a Melastomataceae-galling clade, 3) a leafmining clade A, 4) a leafmining clade B, 5) a Zapyrastra Meyrick clade, and 6) a monobasic lineage represented by Mompha eloisella (Clemens). Ancestral trait reconstructions using the COI phylogeny identified leafmining on Onagraceae as the ancestral state for Momphidae. Our study finds that shifts along three hostplant resource axes (plant taxon, plant tissue type, and larval feeding mode) have contributed to the evolutionary success and diversification of momphids.

Population and colony structure and morphometrics in the queen dimorphic little black ant, Monomorium sp. AZ-02, with a review of queen phenotypes in the genus Monomorium.

The North American little black ant, Monomorium sp. AZ-02 (subfamily Myrmicinae), displays a dimorphism that consists of alate (winged) and ergatoid (wingless) queens. Surveys at our field site in southcentral Arizona, USA, demonstrated that only one queen phenotype (alate or ergatoid) occurred in each colony during the season in which reproductive sexuals were produced. A morphometric analysis demonstrated that ergatoid queens retained all specialized anatomical features of alate queens (except for wings), and that they were significantly smaller and had a lower mass than alate queens. Using eight morphological characters, a discriminant analysis correctly categorized all queens (40 of 40) of both phenotypes. A molecular phylogeny using 420 base pairs of the mitochondrial gene cytochrome oxidase I demonstrated that alate and ergatoid queens are two alternative phenotypes within the species; both phenotypes were intermixed on our phylogeny, and both phenotypes often displayed the same haplotype. A survey of the genus Monomorium (358 species) found that wingless queens (ergatoid queens, brachypterous queens) occur in 42 of 137 species (30.6%) in which the queen has been described. These wingless queen species are geographically and taxonomically widespread as they occur on several continents and in eight species groups, suggesting that winglessness probably arose independently on many occasions in the genus.

Herbivory as an important selective force in the evolution of floral traits and pollinator shifts.

Floral trait evolution is frequently attributed to pollinator-mediated selection but herbivores can play a key role in shaping plant reproductive biology. Here we examine the role of florivores in driving floral trait evolution and pollinator shifts in a recently radiated clade of flowering plants, Oenothera sect. Calylophus We compare florivory by a specialist, internal feeder, Mompha, on closely related hawkmoth- and bee-pollinated species and document variation in damage based on floral traits within sites, species and among species. Our results show that flowers with longer floral tubes and decreased floral flare have increased Mompha damage. Bee-pollinated flowers, which have substantially smaller floral tubes, experience on average 13% less Mompha florivory than do hawkmoth-pollinated flowers. The positive association between tube length and Mompha damage is evident even within sites of some species, suggesting that Mompha can drive trait differentiation at microevolutionary scales. Given that there are at least two independent shifts from hawkmoth to bee pollination in this clade, florivore-mediated selection on floral traits may have played an important role in facilitating morphological changes associated with transitions from hawkmoth to bee pollination.

Taxonomic revision of the genus Prionopelta (Hymenoptera, Formicidae) in the Malagasy region.

In this study we revise the taxonomy of the genus Prionopelta for the Malagasy region, treating seven species, six of which are newly described (Prionopeltalaurae sp. n., Prionopeltaseychelles sp. n., Prionopeltasubtilis sp. n., Prionopeltatalos sp. n., Prionopeltavampira sp. n., Prionopeltaxerosilva sp. n.), and one redescribed (Prionopeltadescarpentriesi Santschi). One species, Prionopeltaseychelles, is restricted to Seychelles, while the six remaining species treated are endemic to Madagascar.

A New Species of Seed-harvester Ant, Pogonomyrmex hoelldobleri (Hymenoptera: Formicidae), from the Mohave and Sonoran Deserts of North America.

Pogonomyrmex magnacanthus Cole was described as a distinct species; unusually large eyes and a high ocular index (maximum eye diameter/head width) were listed as diagnostic characters. However, examination of numerous series of P. magnacanthus revealed that both characters were highly variable, and that these series consisted of P. magnacanthus plus an undescribed species, Pogonomyrmex hoelldobleri Johnson, Overson & Moreau sp. nov. This paper describes all three castes of P. hoelldobleri as well as the alate queen of P mohavensis, which is very similar to that of P. hoelldobleri. A molecular phylogeny that consisted of 3,703 bp from one mitochondrial and five nuclear gene fragments-supported the monophyly of P. hoelldobleri, P. magnacanthus, and P mohavensis. Pogonomyrnex inagnacanthus can be separated from other P. californicus group species based on: (1) its unusually large eyes, (2) a high ocular index, and (3) a malar ratio that is typically < or = 1.0. Pogonomyrmex hoelldobleri can be separated from other P. californicus group species based on the combination of: (1) eyes not unusually large, (2) cephalic rugae not forming circumocular whorls, but rather converging posterior to the eyes, usually near the vertex, (3) mandible with seven teeth, and (4) interrugal spaces on pronotal sides moderately to strongly granulate, dull to weakly shining. Pogonomyrmex mohavensis can be separated from other P. californicus group species based on the combination of: (1) eyes not unusually large, (2) cephalic rugae not forming circumocular whorls, but rather extending more or less directly to the vertex or converging only slightly near the vertex, (3) mandible with six teeth (a seventh sometimes occurs as a denticle between the basal and sub-basal teeth), and (4) interrugal spaces on pronotal sides smooth and shining to weakly punctate and moderately shining. We also provide field observations and distribution maps for P. magnacanthus, P. hoelldobleri, and P. mohavensis, and an updated key to P californicus group species that occur in central and western North America.

Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile).

Ants are some of the most abundant and familiar animals on Earth, and they play vital roles in most terrestrial ecosystems. Although all ants are eusocial, and display a variety of complex and fascinating behaviors, few genomic resources exist for them. Here, we report the draft genome sequence of a particularly widespread and well-studied species, the invasive Argentine ant (Linepithema humile), which was accomplished using a combination of 454 (Roche) and Illumina sequencing and community-based funding rather than federal grant support. Manual annotation of >1,000 genes from a variety of different gene families and functional classes reveals unique features of the Argentine ant's biology, as well as similarities to Apis mellifera and Nasonia vitripennis. Distinctive features of the Argentine ant genome include remarkable expansions of gustatory (116 genes) and odorant receptors (367 genes), an abundance of cytochrome P450 genes (>110), lineage-specific expansions of yellow/major royal jelly proteins and desaturases, and complete CpG DNA methylation and RNAi toolkits. The Argentine ant genome contains fewer immune genes than Drosophila and Tribolium, which may reflect the prominent role played by behavioral and chemical suppression of pathogens. Analysis of the ratio of observed to expected CpG nucleotides for genes in the reproductive development and apoptosis pathways suggests higher levels of methylation than in the genome overall. The resources provided by this genome sequence will offer an abundance of tools for researchers seeking to illuminate the fascinating biology of this emerging model organism.

The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.

Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldiers, resulting in one of the most complex polymorphic caste systems within ants. To begin uncovering the genomic underpinnings of this system, we sequenced the genome of Atta cephalotes using 454 pyrosequencing. One prediction from this ant's lifestyle is that it has undergone genetic modifications that reflect its obligate dependence on the fungus for nutrients. Analysis of this genome sequence is consistent with this hypothesis, as we find evidence for reductions in genes related to nutrient acquisition. These include extensive reductions in serine proteases (which are likely unnecessary because proteolysis is not a primary mechanism used to process nutrients obtained from the fungus), a loss of genes involved in arginine biosynthesis (suggesting that this amino acid is obtained from the fungus), and the absence of a hexamerin (which sequesters amino acids during larval development in other insects). Following recent reports of genome sequences from other insects that engage in symbioses with beneficial microbes, the A. cephalotes genome provides new insights into the symbiotic lifestyle of this ant and advances our understanding of host-microbe symbioses.

Draft genome of the red harvester ant Pogonomyrmex barbatus.

We report the draft genome sequence of the red harvester ant, Pogonomyrmex barbatus. The genome was sequenced using 454 pyrosequencing, and the current assembly and annotation were completed in less than 1 y. Analyses of conserved gene groups (more than 1,200 manually annotated genes to date) suggest a high-quality assembly and annotation comparable to recently sequenced insect genomes using Sanger sequencing. The red harvester ant is a model for studying reproductive division of labor, phenotypic plasticity, and sociogenomics. Although the genome of P. barbatus is similar to other sequenced hymenopterans (Apis mellifera and Nasonia vitripennis) in GC content and compositional organization, and possesses a complete CpG methylation toolkit, its predicted genomic CpG content differs markedly from the other hymenopterans. Gene networks involved in generating key differences between the queen and worker castes (e.g., wings and ovaries) show signatures of increased methylation and suggest that ants and bees may have independently co-opted the same gene regulatory mechanisms for reproductive division of labor. Gene family expansions (e.g., 344 functional odorant receptors) and pseudogene accumulation in chemoreception and P450 genes compared with A. mellifera and N. vitripennis are consistent with major life-history changes during the adaptive radiation of Pogonomyrmex spp., perhaps in parallel with the development of the North American deserts.

Social insects inspire human design.

The international conference 'Social Biomimicry: Insect Societies and Human Design', hosted by Arizona State University, USA, 18-20 February 2010, explored how the collective behaviour and nest architecture of social insects can inspire innovative and effective solutions to human design challenges. It brought together biologists, designers, engineers, computer scientists, architects and businesspeople, with the dual aims of enriching biology and advancing biomimetic design.