Phylogeography and population genetics of a widespread cold-adapted ant, Prenolepis imparis.

As species arise, evolve and diverge, they are shaped by forces that unfold across short and long timescales and at both local and vast geographical scales. It is rare, however, to be able document this history across broad sweeps of time and space in a single species. Here, we report the results of a continental-scale phylogenomic analysis across the entire range of a widespread species. We analysed sequences of 1402 orthologous ultraconserved element (UCE) loci from 75 individuals to identify population genetic structure and historical demographic patterns across the continent-wide range of a cold-adapted ant, the winter ant, Prenolepis imparis. We recovered five well-supported, genetically isolated clades representing lineages that diverged from 8.2-2.2 million years ago. These include: (i) an early diverging lineage located in Florida, (ii) a lineage that spans the southern United States, (iii) populations that extend across the midwestern and northeastern United States, (iv) populations from the western United States and (v) populations in southwestern Arizona and Mexico. Population genetic analyses revealed little or no gene flow among these lineages, but patterns consistent with more recent gene flow among populations within lineages, and localized structure with migration in the western United States. High support for five major geographical lineages and lack of evidence of contemporary gene flow indicate in situ diversification across the species' range, producing relatively ancient lineages that persisted through subsequent climate change and glaciation during the Quaternary.

Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data.

Cryptic species diversity is a major challenge regarding the species-rich community of parasitoids attacking oak gall wasps due to a high degree of sexual dimorphism, morphological plasticity, small size and poorly known biology. As such, we know very little about the number of species present, nor the evolutionary forces responsible for generating this diversity. One hypothesis is that trait diversity in the gall wasps, including the morphology of the galls they induce, has evolved in response to selection imposed by the parasitoid community, with reciprocal selection driving diversification of the parasitoids. Using a rare, continental-scale data set of Sycophila parasitoid wasps reared from 44 species of cynipid galls from 18 species of oak across the USA, we combined mitochondrial DNA barcodes, ultraconserved elements (UCEs), morphological and natural history data to delimit putative species. Using these results, we generate the first large-scale assessment of ecological specialization and host association in this species-rich group, with implications for evolutionary ecology and biocontrol. We find most Sycophila target specific subsets of available cynipid host galls with similar morphologies, and generally attack larger galls. Our results suggest that parasitoid wasps such as Sycophila have adaptations allowing them to exploit particular host trait combinations, while hosts with contrasting traits are resistant to attack. These findings support the tritrophic niche concept for the structuring of plant-herbivore-parasitoid communities.

Protective Benefits of Tending Ants to a Critically Endangered Butterfly.

Ants provide protection to various organisms via myrmecophilous relationships. Most notably, ants and several butterfly species are involved in mainly mutualistic interactions. Previous field studies have shown that butterfly larval survival is increased in the presence of tending ants, suggesting that ants are providing protection against insect predation or parasitism. Here, we conducted a series of timed observational trials under laboratory conditions to assess larval survival and ant protection from insect predators for a myrmecophilous lycaenid butterfly. We focused on a critically endangered butterfly, the Miami blue (Cyclargus thomasi bethunebakeri) (Comstock and Huntington) (Lepidoptera: Lycaenidae), and its most common ant associate, the Florida carpenter ant (Camponotus floridanus) (Buckley) (Hymenoptera: Formicidae), to test this assumption of ant protection. We found that ants provide significant protection to Miami blue larvae, with later instar larvae receiving a higher level of protection due to differences in tending frequencies. These results will aid in informing conservation management and future organism reintroductions for this endangered butterfly.

UCE data reveal multiple origins of rose gallers in North America: Global phylogeny of Diplolepis Geoffroy (Hymenoptera: Cynipidae).

Gall wasps in the genus Diplolepis Geoffroy are specialized herbivores that induce galls exclusively on roses. Despite their wide distribution across the Holarctic, little is known about their evolutionary history. Here we present the first phylogenomic tree of global Diplolepis reconstructed using Ultraconserved Elements (UCEs), resulting in a robust phylogeny based on 757 genes. Results support the existence of two principal clades: a Nearctic stem-galler clade, and a Holarctic leaf-galler clade that further splits into two Palearctic groups and one Nearctic group. This topology is congruent with a previous study based on the mitochondrial gene COI, an unexpected result given the common occurrence of mitonuclear discordance in closely related oak gall wasp lineages. Most Diplolepis species were recovered as reciprocally monophyletic, with some notable exceptions such as the D. polita and the D. ignota complex, for which species boundaries remain unresolved. Historical biogeographic reconstruction was unable to pinpoint the origin of Diplolepis, but confirms two independent incursions into the Nearctic. Ancestral state reconstruction analysis highlights the conservatism of gall location on the host plants, as shifts to different host organs are relatively rare. We suggest that Diplolepis were originally leaf gallers, with a Nearctic stem-galler clade undergoing a major plant organ switch onto rose stems. Host organ switch or reversal is uncommon, which suggests a level of conservatism. Our study showcases the resolving power of UCEs at the species level while also suggesting improvements to advance future Cynipoidea phylogenomics. Our results also highlight the additional sampling needed to clarify taxonomic relationships in the Nearctic and eastern Palearctic regions.

Dominance-diversity relationships in ant communities differ with invasion.

The relationship between levels of dominance and species richness is highly contentious, especially in ant communities. The dominance-impoverishment rule states that high levels of dominance only occur in species-poor communities, but there appear to be many cases of high levels of dominance in highly diverse communities. The extent to which dominant species limit local richness through competitive exclusion remains unclear, but such exclusion appears more apparent for non-native rather than native dominant species. Here we perform the first global analysis of the relationship between behavioral dominance and species richness. We used data from 1,293 local assemblages of ground-dwelling ants distributed across five continents to document the generality of the dominance-impoverishment rule, and to identify the biotic and abiotic conditions under which it does and does not apply. We found that the behavioral dominance-diversity relationship varies greatly, and depends on whether dominant species are native or non-native, whether dominance is considered as occurrence or relative abundance, and on variation in mean annual temperature. There were declines in diversity with increasing dominance in invaded communities, but diversity increased with increasing dominance in native communities. These patterns occur along the global temperature gradient. However, positive and negative relationships are strongest in the hottest sites. We also found that climate regulates the degree of behavioral dominance, but differently from how it shapes species richness. Our findings imply that, despite strong competitive interactions among ants, competitive exclusion is not a major driver of local richness in native ant communities. Although the dominance-impoverishment rule applies to invaded communities, we propose an alternative dominance-diversification rule for native communities.

A global database of ant species abundances.

What forces structure ecological assemblages? A key limitation to general insights about assemblage structure is the availability of data that are collected at a small spatial grain (local assemblages) and a large spatial extent (global coverage). Here, we present published and unpublished data from 51 ,388 ant abundance and occurrence records of more than 2,693 species and 7,953 morphospecies from local assemblages collected at 4,212 locations around the world. Ants were selected because they are diverse and abundant globally, comprise a large fraction of animal biomass in most terrestrial communities, and are key contributors to a range of ecosystem functions. Data were collected between 1949 and 2014, and include, for each geo-referenced sampling site, both the identity of the ants collected and details of sampling design, habitat type, and degree of disturbance. The aim of compiling this data set was to provide comprehensive species abundance data in order to test relationships between assemblage structure and environmental and biogeographic factors. Data were collected using a variety of standardized methods, such as pitfall and Winkler traps, and will be valuable for studies investigating large-scale forces structuring local assemblages. Understanding such relationships is particularly critical under current rates of global change. We encourage authors holding additional data on systematically collected ant assemblages, especially those in dry and cold, and remote areas, to contact us and contribute their data to this growing data set.

Climate mediates the effects of disturbance on ant assemblage structure.

Many studies have focused on the impacts of climate change on biological assemblages, yet little is known about how climate interacts with other major anthropogenic influences on biodiversity, such as habitat disturbance. Using a unique global database of 1128 local ant assemblages, we examined whether climate mediates the effects of habitat disturbance on assemblage structure at a global scale. Species richness and evenness were associated positively with temperature, and negatively with disturbance. However, the interaction among temperature, precipitation and disturbance shaped species richness and evenness. The effect was manifested through a failure of species richness to increase substantially with temperature in transformed habitats at low precipitation. At low precipitation levels, evenness increased with temperature in undisturbed sites, peaked at medium temperatures in disturbed sites and remained low in transformed sites. In warmer climates with lower rainfall, the effects of increasing disturbance on species richness and evenness were akin to decreases in temperature of up to 9°C. Anthropogenic disturbance and ongoing climate change may interact in complicated ways to shape the structure of assemblages, with hot, arid environments likely to be at greatest risk.

Molecular phylogeny and biogeography of the spider ants, genus Leptomyrmex Mayr (Hymenoptera: Formicidae).

This study provides the first phylogenetic reconstruction of the ant genus Leptomyrmex Mayr, a prominent endemic component of rain forest and wet sclerophyll forest in Australia, New Guinea and New Caledonia. Five genes are used to reconstruct phylogeny and estimate of ages of diversification in order to test congruence of the history of nuclear and mitochondrial genes: three protein-coding nuclear genes: arginine kinase (argK, 897 bp), long wavelength rhodopsin (LW Rh, 546 bp) and wingless (Wg, 409 bp), as well as the large subunit ribosomal gene 28S (482 bp) and the mitochondrial gene cytochrome oxidase I (COI, 658 bp). Four different partitioning schemes were tested for optimal resolving power; results show that partitioning by gene, translational pattern and codon position were uniformly favoured over less complex partitions. Nuclear markers showed relatively minor sequence divergence and provided strongly supported topology; phylogeny based solely on mtDNA produced somewhat conflicting topology but offered little power to resolve species complexes. Monophyly of the genus Leptomyrmex was recovered, as was the sister-group relationship of 'micro-' and 'macro-'Leptomyrmex species. Divergence dating analyses estimate that Leptomyrmex arose in the Eocene (stem age ∼ 44 million years ago (ma)), and that the 'macro-' species diverged from the 'micro-' species in the early Oligocene (∼ 31 ma). Diversification of the crown group 'macro-' and 'micro-'Leptomyrmex occurred in the Miocene (∼ 15 ma and 7.9 ma, respectively). New Guinean and New Caledonian lineages appear to have diverged from Australian lineages only recently (∼ 4.7 ma and 10.3 ma, respectively), and the latter clade is inferred to have reached New Caledonia from Australia via long distance dispersal. These results challenge previous hypotheses of Leptomyrmex classification and assumptions about their historical dispersal, but are in agreement with the current knowledge of the geological history of Melanesia.

Effects of prescribed fire and social insects on saproxylic beetles in a subtropical forest.

We tested the immediate and delayed effects of a low-intensity prescribed fire on beetles, ants and termites inhabiting log sections cut from moderately decomposed pine trees in the southeastern United States. We also explored co-occurrence patterns among these insects. Half the logs were placed at a site scheduled for a prescribed fire while the rest were assigned to a neighboring site not scheduled to be burned. We then collected insects emerging from sets of logs collected immediately after the fire as well as after 2, 6, 26 and 52 weeks. The fire had little effect on the number of beetles and ants collected although beetle richness was significantly higher in burned logs two weeks after the fire. Both beetle and ant communities differed between treatments, however, with some species preferring either burned or unburned logs. We found no evidence that subterranean termites (Reticulitermes) were influenced by the fire. Based on co-occurrence analysis, positive associations among insect species were over two times more common than negative associations. This difference was significant overall as well for ant × beetle and beetle × beetle associations. Relatively few significant positive or negative associations were detected between termites and the other insect taxa, however.

Developing a vocabulary and ontology for modeling insect natural history data: example data, use cases, and competency questions.

Insects are possibly the most taxonomically and ecologically diverse class of multicellular organisms on Earth. Consequently, they provide nearly unlimited opportunities to develop and test ecological and evolutionary hypotheses. Currently, however, large-scale studies of insect ecology, behavior, and trait evolution are impeded by the difficulty in obtaining and analyzing data derived from natural history observations of insects. These data are typically highly heterogeneous and widely scattered among many sources, which makes developing robust information systems to aggregate and disseminate them a significant challenge. As a step towards this goal, we report initial results of a new effort to develop a standardized vocabulary and ontology for insect natural history data. In particular, we describe a new database of representative insect natural history data derived from multiple sources (but focused on data from specimens in biological collections), an analysis of the abstract conceptual areas required for a comprehensive ontology of insect natural history data, and a database of use cases and competency questions to guide the development of data systems for insect natural history data. We also discuss data modeling and technology-related challenges that must be overcome to implement robust integration of insect natural history data.

Managed Fire Frequency Significantly Influences the Litter Arthropod Community in Longleaf Pine Flatwoods.

Frequent prescribed burns are essential to pine forest restoration and management. Research studies have assessed effects of prescribed fire and burn frequency on plants and vertebrates, but impacts of fire on terrestrial invertebrate communities are still poorly understood. This case study investigated effects of burning frequency on species richness and community composition of social insects (ants, Hymenoptera: Formicidae and termites, Blattodea: Isoptera) in fire-managed Southern longleaf pine flatwoods in central Florida. Community response to different fire frequencies was assessed: burned annually, every 2 yr, or every 3 yr, 30 yr unburned and 75 yr unburned. Richness was similar across all treatments, but ant community composition and species density significantly differed between frequently burned (1, 2, and 3 yr) and long-unburned (30 and 75 yr) treatments. Long-unburned treatments had higher ant abundance, but the species present were less characteristic of open canopy longleaf pine habitat than ants in frequently burned treatments. The annual burn treatment differed from 2-yr burn in species density, but to a lesser degree. Exotic species abundance was highest in frequently burned sites; only native species were detected in the 75-yr unburned plot. The red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), was detected in all regularly burned plots but not in long-unburned sites. Frequent burning at this site increased habitat suitability for ant species adapted to the sunny, open canopy, and diverse niches characteristic of longleaf pine forest; however, regular fire disturbance also increased the likelihood of exotic ant species establishment.

Breaking out of biogeographical modules: range expansion and taxon cycles in the hyperdiverse ant genus Pheidole.

AIM: We sought to reconstruct the biogeographical structure and dynamics of a hyperdiverse ant genus, Pheidole, and to test several predictions of the taxon cycle hypothesis. Using large datasets on Pheidole geographical distributions and phylogeny, we (1) inferred patterns of biogeographical modularity (clusters of areas with similar faunal composition), (2) tested whether species in open habitats are more likely to be expanding their range beyond module boundaries, and (3) tested whether there is a bias of lineage flow from high- to low-diversity areas. LOCATION: The Old World. METHODS: We compiled and jointly analysed a comprehensive database of Pheidole geographical distributions, the ecological affinities of different species, and a multilocus phylogeny of the Old World radiation. We used network modularity methods to infer biogeographical structure in the genus and comparative methods to evaluate the hypotheses. RESULTS: The network analysis identified eight biogeographical modules, and a suite of species with anomalous ranges that are statistically more likely to occur in open habitat, supporting the hypothesis that open habitats promote range expansion. Phylogenetic analysis shows evidence for a cascade pattern of colonization from Asia to New Guinea to the Pacific, but no 'upstream' colonization in the reverse direction. MAIN CONCLUSIONS: The distributions of Pheidole lineages in the Old World are highly modular, with modules generally corresponding to biogeographical regions inferred in other groups of organisms. However, some lineages have expanded their ranges across module boundaries, and these species are more likely to be adapted to open habitats rather than interior forest. In addition, there is a cascade pattern of dispersal from higher to lower diversity areas during these range expansions. Our findings are consistent with the taxon cycle hypothesis, although they do not rule out alternative interpretations.

Tracing the rise of ants - out of the ground.

The evolution of ants (Hymenoptera: Formicidae) is increasingly well-understood due to recent phylogenetic analyses, along with estimates of divergence times and diversification rates. Yet, leading hypotheses regarding the ancestral habitat of ants conflict with new findings that early ant lineages are cryptic and subterranean. Where the ants evolved, in respect to habitat, and how habitat shifts took place over time have not been formally tested. Here, we reconstruct the habitat transitions of crown-group ants through time, focusing on where they nest and forage (in the canopy, litter, or soil). Based on ancestral character reconstructions, we show that in contrast to the current consensus based on verbal arguments that ants evolved in tropical leaf litter, the soil is supported as the ancestral stratum of all ants. We also find subsequent movements up into the litter and, in some cases, into the canopy. Given the global importance of ants, because of their diversity, ecological influence and status as the most successful eusocial lineage on Earth, understanding the early evolution of this lineage provides insight into the factors that made this group so successful today.

A jungle in there: bacteria in belly buttons are highly diverse, but predictable.

The belly button is one of the habitats closest to us, and yet it remains relatively unexplored. We analyzed bacteria and arachaea from the belly buttons of humans from two different populations sampled within a nation-wide citizen science project. We examined bacterial and archaeal phylotypes present and their diversity using multiplex pyrosequencing of 16S rDNA libraries. We then tested the oligarchy hypothesis borrowed from tropical macroecology, namely that the frequency of phylotypes in one sample of humans predicts its frequency in another independent sample. We also tested the predictions that frequent phylotypes (the oligarchs) tend to be common when present, and tend to be more phylogenetically clustered than rare phylotypes. Once rarefied to four hundred reads per sample, bacterial communities from belly buttons proved to be at least as diverse as communities known from other skin studies (on average 67 bacterial phylotypes per belly button). However, the belly button communities were strongly dominated by a few taxa: only 6 phylotypes occurred on >80% humans. While these frequent bacterial phylotypes (the archaea were all rare) are a tiny part of the total diversity of bacteria in human navels (<0.3% of phylotypes), they constitute a major portion of individual reads (~1/3), and are predictable among independent samples of humans, in terms of both the occurrence and evolutionary relatedness (more closely related than randomly drawn equal sets of phylotypes). Thus, the hypothesis that "oligarchs" dominate diverse assemblages appears to be supported by human-associated bacteria. Although it remains difficult to predict which species of bacteria might be found on a particular human, predicting which species are most frequent (or rare) seems more straightforward, at least for those species living in belly buttons.

Shuffling leaf litter samples produces more accurate and precise snapshots of terrestrial arthropod community composition.

Understanding the accuracy of sampling techniques is critical to accurate interpretation of local and global ecological patterns. Over the past 20 yr, Winkler leaf litter extractors have become one of the most common techniques used to collect terrestrial arthropods. Although the original description of this technique recommends the use of disturbance during extraction to increase extraction efficiency, most published studies do not follow this recommendation. Here we test experimentally how disturbing, or "shuffling" leaf litter during extraction affects collection efficiency for four groups of arthropods: ants, micro-Hymenoptera, beetles, and spiders. Our results show that extraction efficiency for abundance and richness of ants is increased with disturbance. Disturbance also improves extraction efficiency for beetle abundance, but does not affect micro-Hymenoptera and spider abundance or richness. Significantly, our results also demonstrate that shuffling litter can greatly reduce the variability of extraction efficiency between different sites. Because of this greater efficiency, we recommend use of the shuffling technique, when sampling leaf litter via Winkler extractors to maximize the collection of ants and beetles, especially for studies that compare abundance and richness across multiple sites.