Chewing through challenges: Exploring the evolutionary pathways to wood-feeding in insects.

Decaying wood, while an abundant and stable resource, presents considerable nutritional challenges due to its structural rigidity, chemical recalcitrance, and low nitrogen content. Despite these challenges, certain insect lineages have successfully evolved saproxylophagy (consuming and deriving sustenance from decaying wood), impacting nutrient recycling in ecosystems and carbon sequestration dynamics. This study explores the uneven phylogenetic distribution of saproxylophagy across insects and delves into the evolutionary origins of this trait in disparate insect orders. Employing a comprehensive analysis of gut microbiome data, from both saproxylophagous insects and their non-saproxylophagous relatives, including new data from unexplored wood-feeding insects, this Hypothesis paper discusses the broader phylogenetic context and potential adaptations necessary for this dietary specialization. The study proposes the "Detritivore-First Hypothesis," suggesting an evolutionary pathway to saproxylophagy through detritivory, and highlights the critical role of symbiotic gut microbiomes in the digestion of decaying wood.

First rhyncaphytoptine mite (Eriophyoidea, Diptilomiopidae) parasitizing American hazelnut (Corylus americana): molecular identification, confocal microscopy, and phylogenetic position.

The plant genus Corylus is an economically important crop, valued especially for its nuts. Numerous pathogens and harmful phytophagous arthropods are known to damage hazelnuts. We report on a new eriophyoid mite, Rhyncaphytoptus corylivagrans n. sp., and the first record of Coptophylla lamimani both collected from leaves of American hazelnut (Corylus americana) in North Carolina, USA. Including our new data, the complex of eriophyoids from Corylus comprises 15 species from three families: Phytoptidae (2 spp.), Eriophyidae (11 spp.), and Diptilomiopidae (2 spp.). We obtained sequences of three genes (Cox1, D1-D5 28S, and ITS1-5.8S-ITS2), applied BLAST and tree-based approaches for identification of R. corylivagrans n. sp., and performed the first molecular phylogenetic analysis focused on Rhyncaphytoptinae. Among the three genes, Cox1 showed better power when used for BLAST searches. Combined molecular phylogenetic analyses inferred R. corylivagrans n. sp. as sister to R. betulae, determined several moderately supported host-specific lineages of rhyncaphytoptines, and indicated a close relationship of the new species with members of the genus Rhinotergum. In two Rhinotergum spp. from Rosaceae, confocal microscopy revealed a new structure, the needle-like anterior process of the prodorsal shield, which is absent in R. corylivagrans n. sp. Additionally, the elements of the anal secretory apparatus presumably associated with silk-production and hypothesized as a synapomorphy of Eriophyoidea, were detected in the new species, providing the first documented report of this structure in Diptilomiopidae. Our study contributes to knowledge on the biodiversity of phytoparasites associated with hazelnuts and calls for future comparative phylogenetics of Diptilomiopidae.

Oxidative damage increases with degree of simulated bacterial infection, but not ectoparasitism, in tree swallow nestlings.

The purpose of mounting an immune response is to destroy pathogens, but this response comes at a physiological cost, including the generation of oxidative damage. However, many studies on the effects of immune challenges employ a single high dose of a simulated infection, meaning that the consequences of more mild immune challenges are poorly understood. We tested whether the degree of immunological challenge in tree swallows (Tachycineta bicolor) affects oxidative physiology and body mass, and whether these metrics correlate with parasitic nest mite load. We injected 14 day old nestlings with 0, 0.01, 0.1 or 1 mg lipopolysaccharide (LPS) per kg body mass, then collected a blood sample 24 h later to quantify multiple physiological metrics, including oxidative damage (i.e. d-ROMs), circulating amounts of triglyceride and glycerol, and levels of the acute phase protein haptoglobin. After birds had fledged, we identified and counted parasitic nest mites (Dermanyssus spp. and Ornithonyssus spp.). We found that only nestlings injected with 1 mg LPS kg-1 body mass, which is a common dosage in ecoimmunological studies, lost more body mass than individuals from other treatment groups. However, every dose of LPS resulted in a commensurate increase in oxidative damage. Parasitic mite abundance had no effect on oxidative damage across treatments. The amount of oxidative damage correlated with haptoglobin levels, suggesting compensatory mechanisms to limit self-damage during an immune response. We conclude that while only the highest-intensity immune challenges resulted in costs related to body mass, even low-intensity immune challenges result in detectable increases in oxidative damage.

Venus Flytrap Rarely Traps Its Pollinators.

Because carnivorous plants rely on arthropods as pollinators and prey, they risk consuming would-be mutualists. We examined this potential conflict in the Venus flytrap (Dionaea muscipula), whose pollinators were previously unknown. Diverse arthropods from two classes and nine orders visited flowers; 56% of visitors carried D. muscipula pollen, often mixed with pollen of coflowering species. Within this diverse, generalized community, certain bee and beetle species appear to be the most important pollinators, on the basis of their abundance, pollen load size, and pollen fidelity. Dionaea muscipula prey spanned four invertebrate classes and 11 orders; spiders, beetles, and ants were most common. At the family and species levels, few taxa were shared between traps and flowers, yielding a near-zero value of niche overlap for these potentially competing structures. Spatial separation of traps and flowers may contribute to partitioning the invertebrate community between nutritional and reproductive functions in D. muscipula.

Multistate Infestation with the Exotic Disease-Vector Tick Haemaphysalis longicornis - United States, August 2017-September 2018.

Haemaphysalis longicornis is a tick indigenous to eastern Asia and an important vector of human and animal disease agents, resulting in such outcomes as human hemorrhagic fever and reduction of production in dairy cattle by 25%. H. longicornis was discovered on a sheep in New Jersey in August 2017 (1). This was the first detection in the United States outside of quarantine. In the spring of 2018, the tick was again detected at the index site, and later, in other counties in New Jersey, in seven other states in the eastern United States, and in Arkansas. The hosts included six species of domestic animals, six species of wildlife, and humans. To forestall adverse consequences in humans, pets, livestock, and wildlife, several critical actions are indicated, including expanded surveillance to determine the evolving distribution of H. longicornis, detection of pathogens that H. longicornis currently harbors, determination of the capacity of H. longicornis to serve as a vector for a range of potential pathogens, and evaluation of effective agents and methods for the control of H. longicornis.

Invertebrate community response to coarse woody debris removal for bioenergy production from intensively managed forests.

Increased market viability of harvest residues as forest bioenergy feedstock may escalate removal of coarse woody debris in managed forests. Meanwhile, many forest invertebrates use coarse woody debris for cover, food, and reproduction. Few studies have explicitly addressed effects of operational-scale woody biomass harvesting on invertebrates following clearcutting. Therefore, we measured invertebrate community response to large-scale harvest residue removal and micro-site manipulations of harvest residue availability in recently clearcut, intensively managed loblolly pine (Pinus taeda) forests in North Carolina (NC; n = 4) and Georgia (GA; n = 4), USA. We captured 39,794 surface-active invertebrates representing 171 taxonomic groups using pitfall traps situated among micro-site locations (i.e., purposefully retained piles of hardwood stems and piles of conifer stems and areas without coarse woody debris in NC; windrows and no windrows in GA). Micro-site locations were located within six, large-scale treatments (7.16-14.3 ha) in clearcuts. Large-scale treatments represented intensive harvest residue removal, 15% and 30% harvest residue retention, and no harvest residue removal. In NC, ground beetles (Coleoptera: Carabidae) and crickets (Orthoptera: Gryllidae) were three times more abundant in treatments with no harvest residue removal than those with the most intensive harvest residue removal and were reduced in treatments that retained 15% or 30% of harvest residues, although not significantly. Invertebrate taxa richness was greater at micro-site locations with retained hardwood and pine (Pinus spp.) harvest residues than those with minimal amounts of coarse woody debris. In both states, relative abundances of several invertebrate taxa, including cave crickets (Orthoptera: Rhaphidophoridae), fungus gnats (Diptera: Mycetophilidae and Sciaridae), millipedes (Diplopoda), and wood roaches (Blattodea: Ectobiidae), were greater at micro-site locations with retained harvest residues than those with minimal coarse woody debris. Intensified woody biomass harvesting without retention of ≥15% of harvest residue volume may reduce invertebrate taxa richness and abundances of some key invertebrate taxa in regenerating stands. Further, harvest residue management during and after woody biomass harvesting may be an important consideration for maintaining invertebrate diversity and conserving invertebrates that are influential in the maintenance of ecosystem function and integrity in young forests.

The diversity of arthropods in homes across the United States as determined by environmental DNA analyses.

We spend most of our lives inside homes, surrounded by arthropods that impact our property as pests and our health as disease vectors and producers of sensitizing allergens. Despite their relevance to human health and well-being, we know relatively little about the arthropods that exist in our homes and the factors structuring their diversity. As previous work has been limited in scale by the costs and time associated with collecting arthropods and the subsequent morphological identification, we used a DNA-based method for investigating the arthropod diversity in homes via high-throughput marker gene sequencing of home dust. Settled dust samples were collected by citizen scientists from both inside and outside more than 700 homes across the United States, yielding the first continental-scale estimates of arthropod diversity associated with our residences. We were able to document food webs and previously unknown geographic distributions of diverse arthropods - from allergen producers to invasive species and nuisance pests. Home characteristics, including the presence of basements, home occupants and surrounding land use, were more useful than climate parameters in predicting arthropod diversity in homes. These noninvasive, scalable tools and resultant findings not only provide the first continental-scale maps of household arthropod diversity, but our analyses also provide valuable baseline information on arthropod allergen exposures and the distributions of invasive pests inside homes.

Exoskeletons and economics: indoor arthropod diversity increases in affluent neighbourhoods.

In urban ecosystems, socioeconomics contribute to patterns of biodiversity. The 'luxury effect', in which wealthier neighbourhoods are more biologically diverse, has been observed for plants, birds, bats and lizards. Here, we used data from a survey of indoor arthropod diversity (defined throughout as family-level richness) from 50 urban houses and found that house size, surrounding vegetation, as well as mean neighbourhood income best predict the number of kinds of arthropods found indoors. Our finding, that homes in wealthier neighbourhoods host higher indoor arthropod diversity (consisting of primarily non-pest species), shows that the luxury effect can extend to the indoor environment. The effect of mean neighbourhood income on indoor arthropod diversity was particularly strong for individual houses that lacked high surrounding vegetation ground cover, suggesting that neighbourhood dynamics can compensate for local choices of homeowners. Our work suggests that the management of neighbourhoods and cities can have effects on biodiversity that can extend from trees and birds all the way to the arthropod life in bedrooms and basements.

Episodic radiations in the fly tree of life.

Flies are one of four superradiations of insects (along with beetles, wasps, and moths) that account for the majority of animal life on Earth. Diptera includes species known for their ubiquity (Musca domestica house fly), their role as pests (Anopheles gambiae malaria mosquito), and their value as model organisms across the biological sciences (Drosophila melanogaster). A resolved phylogeny for flies provides a framework for genomic, developmental, and evolutionary studies by facilitating comparisons across model organisms, yet recent research has suggested that fly relationships have been obscured by multiple episodes of rapid diversification. We provide a phylogenomic estimate of fly relationships based on molecules and morphology from 149 of 157 families, including 30 kb from 14 nuclear loci and complete mitochondrial genomes combined with 371 morphological characters. Multiple analyses show support for traditional groups (Brachycera, Cyclorrhapha, and Schizophora) and corroborate contentious findings, such as the anomalous Deuterophlebiidae as the sister group to all remaining Diptera. Our findings reveal that the closest relatives of the Drosophilidae are highly modified parasites (including the wingless Braulidae) of bees and other insects. Furthermore, we use micro-RNAs to resolve a node with implications for the evolution of embryonic development in Diptera. We demonstrate that flies experienced three episodes of rapid radiation--lower Diptera (220 Ma), lower Brachycera (180 Ma), and Schizophora (65 Ma)--and a number of life history transitions to hematophagy, phytophagy, and parasitism in the history of fly evolution over 260 million y.

Correction: A novel power-amplified jumping behavior in larval beetles (Coleoptera: Laemophloeidae).

[This corrects the article DOI: 10.1371/journal.pone.0256509.].

Redescription of Dentifibula viburni (Felt) (Diptera: Cecidomyiidae) and review of the genus.

Dentifibula viburni (Felt) (Diptera: Cecidomyiidae), type species of Dentifibula Felt, is redescribed with illustrations and compared with its congeners. The genus is differentiated from the generally similar Lestodiplosis Kieffer. As far as presently known, larvae of Dentifibula prey on Diaspididae (Hemiptera: Coccoidea). The nine other species of Dentifibula are diagnosed. Dentifibula ceylanica Felt is removed from synonymy under Dentifibula obtusiloba Felt.

A novel power-amplified jumping behavior in larval beetles (Coleoptera: Laemophloeidae).

Larval insects use many methods for locomotion. Here we describe a previously unknown jumping behavior in a group of beetle larvae (Coleoptera: Laemophloeidae). We analyze and describe this behavior in Laemophloeus biguttatus and provide information on similar observations for another laemophloeid species, Placonotus testaceus. Laemophloeus biguttatus larvae precede jumps by arching their body while gripping the substrate with their legs over a period of 0.22 ± 0.17s. This is followed by a rapid ventral curling of the body after the larvae releases its grip that launches them into the air. Larvae reached takeoff velocities of 0.47 ± 0.15 m s-1 and traveled 11.2 ± 2.8 mm (1.98 ± 0.8 body lengths) horizontally and 7.9 ± 4.3 mm (1.5 ± 0.9 body lengths) vertically during their jumps. Conservative estimates of power output revealed that some but not all jumps can be explained by direct muscle power alone, suggesting Laemophloeus biguttatus may use a latch-mediated spring actuation mechanism (LaMSA) in which interaction between the larvae's legs and the substrate serves as the latch. MicroCT scans and SEM imaging of larvae did not reveal any notable modifications that would aid in jumping. Although more in-depth experiments could not be performed to test hypotheses on the function of these jumps, we posit that this behavior is used for rapid locomotion which is energetically more efficient than crawling the same distance to disperse from their ephemeral habitat. We also summarize and discuss jumping behaviors among insect larvae for additional context of this behavior in laemophloeid beetles.

Single-copy nuclear genes resolve the phylogeny of the holometabolous insects.

BACKGROUND: Evolutionary relationships among the 11 extant orders of insects that undergo complete metamorphosis, called Holometabola, remain either unresolved or contentious, but are extremely important as a context for accurate comparative biology of insect model organisms. The most phylogenetically enigmatic holometabolan insects are Strepsiptera or twisted wing parasites, whose evolutionary relationship to any other insect order is unconfirmed. They have been controversially proposed as the closest relatives of the flies, based on rDNA, and a possible homeotic transformation in the common ancestor of both groups that would make the reduced forewings of Strepsiptera homologous to the reduced hindwings of Diptera. Here we present evidence from nucleotide sequences of six single-copy nuclear protein coding genes used to reconstruct phylogenetic relationships and estimate evolutionary divergence times for all holometabolan orders. RESULTS: Our results strongly support Hymenoptera as the earliest branching holometabolan lineage, the monophyly of the extant orders, including the fleas, and traditionally recognized groupings of Neuropteroidea and Mecopterida. Most significantly, we find strong support for a close relationship between Coleoptera (beetles) and Strepsiptera, a previously proposed, but analytically controversial relationship. Exploratory analyses reveal that this relationship cannot be explained by long-branch attraction or other systematic biases. Bayesian divergence times analysis, with reference to specific fossil constraints, places the origin of Holometabola in the Carboniferous (355 Ma), a date significantly older than previous paleontological and morphological phylogenetic reconstructions. The origin and diversification of most extant insect orders began in the Triassic, but flourished in the Jurassic, with multiple adaptive radiations producing the astounding diversity of insect species for which these groups are so well known. CONCLUSION: These findings provide the most complete evolutionary framework for future comparative studies on holometabolous model organisms and contribute strong evidence for the resolution of the 'Strepsiptera problem', a long-standing and hotly debated issue in insect phylogenetics.

Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology.

BACKGROUND: Phylogenetic analyses provide a framework for examining the evolution of morphological and molecular diversity, interpreting patterns in biogeography, and achieving a stable classification. The generic and suprageneric relationships within mosquitoes (Diptera: Culicidae) are poorly resolved, making these subjects difficult to address. RESULTS: We carried out maximum parsimony and maximum likelihood, including Bayesian, analyses on a data set consisting of six nuclear genes and 80 morphological characters to assess their ability to resolve relationships among 25 genera. We also estimated divergence times based on sequence data and fossil calibration points, using Bayesian relaxed clock methods. Strong support was recovered for the basal position and monophyly of the subfamily Anophelinae and the tribes Aedini and Sabethini of subfamily Culicinae. Divergence times for major culicid lineages date to the early Cretaceous. CONCLUSIONS: Deeper relationships within the family remain poorly resolved, suggesting the need for additional taxonomic sampling. Our results support the notion of rapid radiations early in the diversification of mosquitoes.

Ecology of sleeping: the microbial and arthropod associates of chimpanzee beds.

The indoor environment created by the construction of homes and other buildings is often considered to be uniquely different from other environments. It is composed of organisms that are less diverse than those of the outdoors and strongly sourced by, or dependent upon, human bodies. Yet, no one has ever compared the composition of species found in contemporary human homes to that of other structures built by mammals, including those of non-human primates. Here we consider the microbes and arthropods found in chimpanzee beds, relative to the surrounding environment (n = 41 and 15 beds, respectively). Based on the study of human homes, we hypothesized that the microbes found in chimpanzee beds would be less diverse than those on nearby branches and leaves and that their beds would be primarily composed of body-associated organisms. However, we found that differences between wet and dry seasons and elevation above sea level explained nearly all of the observed variation in microbial diversity and community structure. While we can identify the presence of a chimpanzee based on the assemblage of bacteria, the dominant signal is that of environmental microbes. We found just four ectoparasitic arthropod specimens, none of which appears to be specialized on chimpanzees or their structures. These results suggest that the life to which chimpanzees are exposed while in their beds is predominately the same as that of the surrounding environment.

The Habitats Humans Provide: Factors affecting the diversity and composition of arthropods in houses.

The indoor biome is a novel habitat which recent studies have shown exhibit not only high microbial diversity, but also high arthropod diversity. Here, we analyze findings from a survey of 50 houses (southeastern USA) within the context of additional survey data concerning house and room features, along with resident behavior, to explore how arthropod diversity and community composition are influenced by physical aspects of rooms and their usage, as well as the lifestyles of human residents. We found that indoor arthropod diversity is strongly influenced by access to the outdoors and carpeted rooms hosted more types of arthropods than non-carpeted rooms. Arthropod communities were similar across most room types, but basements exhibited more unique community compositions. Resident behavior such as house tidiness, pesticide usage, and pet ownership showed no significant influence on arthropod community composition. Arthropod communities across all rooms in houses exhibit trophic structure-with both generalized predators and scavengers included in the most frequently found groups. These findings suggest that indoor arthropods serve as a connection to the outdoors, and that there is still much yet to be discovered about their impact on indoor health and the unique ecological dynamics within our homes.

Description of a new species of Thevenetimyia (Diptera: Bombyliidae) from Madagascar, with a revised checklist of Madagascan bee fly fauna.

Madagascar is an island known for its richness of endemic species, including flies. Only eight genera of bee flies (Bombyliidae), including 17 described species (the majority of which are in the subfamily Anthracinae), are known from Madagascar. Here we describe a new species of Bombyliidae from Madagascar, Thevenetimyia spinosavus Maass & Bertone sp. nov. This fly represents the first record of the genus Thevenetimyia from Madagascar and the second species recorded in the Afrotropical Region. A revised checklist of Bombyliidae in Madagascar is provided, along with an appendix of associated literature. The known bee fly species likely represent only a fraction of the true diversity on the island, which has been relatively well sampled through extensive Malaise trapping of flies in Madagascar over the past decade.

Arthropods of the great indoors: characterizing diversity inside urban and suburban homes.

Although humans and arthropods have been living and evolving together for all of our history, we know very little about the arthropods we share our homes with apart from major pest groups. Here we surveyed, for the first time, the complete arthropod fauna of the indoor biome in 50 houses (located in and around Raleigh, North Carolina, USA). We discovered high diversity, with a conservative estimate range of 32-211 morphospecies, and 24-128 distinct arthropod families per house. The majority of this indoor diversity (73%) was made up of true flies (Diptera), spiders (Araneae), beetles (Coleoptera), and wasps and kin (Hymenoptera, especially ants: Formicidae). Much of the arthropod diversity within houses did not consist of synanthropic species, but instead included arthropods that were filtered from the surrounding landscape. As such, common pest species were found less frequently than benign species. Some of the most frequently found arthropods in houses, such as gall midges (Cecidomyiidae) and book lice (Liposcelididae), are unfamiliar to the general public despite their ubiquity. These findings present a new understanding of the diversity, prevalence, and distribution of the arthropods in our daily lives. Considering their impact as household pests, disease vectors, generators of allergens, and facilitators of the indoor microbiome, advancing our knowledge of the ecology and evolution of arthropods in homes has major economic and human health implications.

Utilizing descriptive statements from the biodiversity heritage library to expand the Hymenoptera Anatomy Ontology.

Hymenoptera, the insect order that includes sawflies, bees, wasps, and ants, exhibits an incredible diversity of phenotypes, with over 145,000 species described in a corpus of textual knowledge since Carolus Linnaeus. In the absence of specialized training, often spanning decades, however, these articles can be challenging to decipher. Much of the vocabulary is domain-specific (e.g., Hymenoptera biology), historically without a comprehensive glossary, and contains much homonymous and synonymous terminology. The Hymenoptera Anatomy Ontology was developed to surmount this challenge and to aid future communication related to hymenopteran anatomy, as well as provide support for domain experts so they may actively benefit from the anatomy ontology development. As part of HAO development, an active learning, dictionary-based, natural language recognition tool was implemented to facilitate Hymenoptera anatomy term discovery in literature. We present this tool, referred to as the 'Proofer', as part of an iterative approach to growing phenotype-relevant ontologies, regardless of domain. The process of ontology development results in a critical mass of terms that is applied as a filter to the source collection of articles in order to reveal term occurrence and biases in natural language species descriptions. Our results indicate that taxonomists use domain-specific terminology that follows taxonomic specialization, particularly at superfamily and family level groupings and that the developed Proofer tool is effective for term discovery, facilitating ontology construction.

Matching arthropod anatomy ontologies to the Hymenoptera Anatomy Ontology: results from a manual alignment.

Matching is an important step for increasing interoperability between heterogeneous ontologies. Here, we present alignments we produced as domain experts, using a manual mapping process, between the Hymenoptera Anatomy Ontology and other existing arthropod anatomy ontologies (representing spiders, ticks, mosquitoes and Drosophila melanogaster). The resulting alignments contain from 43 to 368 mappings (correspondences), all derived from domain-expert input. Despite the many pairwise correspondences, only 11 correspondences were found in common between all ontologies, suggesting either major intrinsic differences between each ontology or gaps in representing each group's anatomy. Furthermore, we compare our findings with putative correspondences from Bioportal (derived from LOOM software) and summarize the results in a total evidence alignment. We briefly discuss characteristics of the ontologies and issues with the matching process.