Michelle D. Trautwein

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.

Advances in Insect Phylogeny at the Dawn of the Postgenomic Era

Most species on Earth are insects and thus, understanding their evolutionary relationships is key to understanding the evolution of life. Insect relationships are increasingly well supported, due largely to technological advances in molecular sequencing and phylogenetic computational analysis. In this postgenomic era, insect systematics will be furthered best by integrative methods aimed at hypothesis corroboration from molecular, morphological, and paleontological evidence. This review of the current consensus of insect relationships provides a foundation for comparative study and offers a framework to evaluate incoming genomic evidence. Notable recent phylogenetic successes include the resolution of Holometabola, including the identification of the enigmatic Strepsiptera as a beetle relative and the early divergence of Hymenoptera; the recognition of hexapods as a crustacean lineage within Pancrustacea; and the elucidation of Dictyoptera orders, with termites placed as social cockroaches. Regions of the tree that require further investigation include the earliest winged insects (Palaeoptera) and Polyneoptera (orthopteroid lineages).

Ubiquity and Diversity of Human-Associated Demodex Mites

Demodex mites are a group of hair follicle and sebaceous gland-dwelling species. The species of these mites found on humans are arguably the animals with which we have the most intimate interactions. Yet, their prevalence and diversity have been poorly explored. Here we use a new molecular method to assess the occurrence of Demodex mites on humans. In addition, we use the 18S rRNA gene (18S rDNA) to assess the genetic diversity and evolutionary history of Demodex lineages. Within our samples, 100% of people over 18 years of age appear to host at least one Demodex species, suggesting that Demodex mites may be universal associates of adult humans. A phylogenetic analysis of 18S rDNA reveals intraspecific structure within one of the two named human-associated Demodex species, D. brevis. The D. brevis clade is geographically structured, suggesting that new lineages are likely to be discovered as humans from additional geographic regions are sampled.

Power, resolution and bias: recent advances in insect phylogeny driven by the genomic revolution.

Our understanding on the phylogenetic relationships of insects has been revolutionised in the last decade by the proliferation of next generation sequencing technologies (NGS). NGS has allowed insect systematists to assemble very large molecular datasets that include both model and non-model organisms. Such datasets often include a large proportion of the total number of protein coding sequences available for phylogenetic comparison. We review some early entomological phylogenomic studies that employ a range of different data sampling protocols and analyses strategies, illustrating a fundamental renaissance in our understanding of insect evolution all driven by the genomic revolution. The analysis of phylogenomic datasets is challenging because of their size and complexity, and it is obvious that the increasing size alone does not ensure that phylogenetic signal overcomes systematic biases in the data. Biases can be due to various factors such as the method of data generation and assembly, or intrinsic biological feature of the data per se, such as similarities due to saturation or compositional heterogeneity. Such biases often cause violations in the underlying assumptions of phylogenetic models. We review some of the bioinformatics tools available and being developed to detect and minimise systematic biases in phylogenomic datasets. Phylogenomic-scale data coupled with sophisticated analyses will revolutionise our understanding of insect functional genomics. This will illuminate the relationship between the vast range of insect phenotypic diversity and underlying genetic diversity. In combination with rapidly developing methods to estimate divergence times, these analyses will also provide a compelling view of the rates and patterns of lineagenesis (birth of lineages) over the half billion years of insect evolution.

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.

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.

Overcoming the effects of rogue taxa: Evolutionary relationships of the bee flies.

Bombyliidae (5000 sp.), or bee flies, are a lower brachyceran family of flower-visiting flies that, as larvae, act as parasitoids of other insects. The evolutionary relationships are known from a morphological analysis that yielded minimal support for higher-level groupings. We use the protein-coding gene CAD and 28S rDNA to determine phylogeny and to test the monophyly of existing subfamilies, the divisions Tomophtalmae, and ‘the sand chamber subfamilies’. Additionally, we demonstrate that consensus networks can be used to identify rogue taxa in a Bayesian framework. Pruning rogue taxa post-analysis from the final tree distribution results in increased posterior probabilities. We find 8 subfamilies to be monophyletic and the subfamilies Heterotropinae and Mythicomyiinae to be the earliest diverging lineages. The large subfamily Bombyliinae is found to be polyphyletic and our data does not provide evidence for the monophyly of Tomophthalmae or the ‘sand chamber subfamilies’.

Global divergence of the human follicle mite Demodex folliculorum: Persistent associations between host ancestry and mite lineages

Significance Mites live in human hair follicles and have been implicated in medically important skin disorders, but we know surprisingly little about these residents of our skin. By analyzing the variation segregating among 241 mite sequences isolated from 70 human hosts, we showed that hosts with different regional ancestries harbor distinct lineages of mites and that these associations can persist despite generations spent in a new geographic region. These results suggest that some mite populations are better able to survive and reproduce on hosts from certain geographic regions. Improving our understanding of human follicle mites promises to shed light on human evolution and to provide important contextual information for their role in human health. Microscopic mites of the genus Demodex live within the hair follicles of mammals and are ubiquitous symbionts of humans, but little molecular work has been done to understand their genetic diversity or transmission. Here we sampled mite DNA from 70 human hosts of diverse geographic ancestries and analyzed 241 sequences from the mitochondrial genome of the species Demodex folliculorum. Phylogenetic analyses recovered multiple deep lineages including a globally distributed lineage common among hosts of European ancestry and three lineages that primarily include hosts of Asian, African, and Latin American ancestry. To a great extent, the ancestral geography of hosts predicted the lineages of mites found on them; 27% of the total molecular variance segregated according to the regional ancestries of hosts. We found that D. folliculorum populations are stable on an individual over the course of years and that some Asian and African American hosts maintain specific mite lineages over the course of years or generations outside their geographic region of birth or ancestry. D. folliculorum haplotypes were much more likely to be shared within families and between spouses than between unrelated individuals, indicating that transmission requires close contact. Dating analyses indicated that D. folliculorum origins may predate modern humans. Overall, D. folliculorum evolution reflects ancient human population divergences, is consistent with an out-of-Africa dispersal hypothesis, and presents an excellent model system for further understanding the history of human movement.

Taxon sampling to address an ancient rapid radiation: a supermatrix phylogeny of early brachyceran flies (Diptera): Diptera evolution and supermatrix

Early diverging brachyceran fly lineages underwent a rapid radiation approximately 180 Ma, coincident in part with the origin of flowering plants. This region of the fly tree includes 25 000 described extant species with diverse ecological roles such as blood‐feeding (haematophagy), parasitoidism, predation, pollination and wood‐feeding (xylophagy). Early diverging brachyceran lineages were once considered a monophyletic group of families called Orthorrhapha, based on the shared character of a longitudinal break in the pupal skin made during the emergence of the adult. Yet other morphological and molecular evidence generally supports a paraphyletic arrangement of ‘Orthorrhapha’, with strong support for one orthorrhaphan lineage – dance flies and relatives – as the closest relative to all higher flies (Cyclorrhapha), together called Eremoneura. In order to establish a comprehensive estimate of the relationships among orthorrhaphan lineages using a thorough sample of publicly available data, we compiled and analysed a dataset including 1217 taxa representing major lineages and 20 molecular markers. Our analyses suggest that ‘Orthorrhapha’ excluding Eremoneura is not monophyletic; instead, we recover two main lineages of early brachyceran flies: Homeodactyla and Heterodactyla. Homeodactyla includes Nemestrinoidea (uniting two parasitic families Acroceridae + Nemestrinidae) as the closest relatives to the large SXT clade, comprising Stratiomyomorpha, Xylophagidae and Tabanomorpha. Heterodactyla includes Bombyliidae with a monophyletic Asiloidea (exclusive of Bombyliidae) as the closest relatives to Eremoneura. Reducing missing data, modifying the distribution of genes across taxa, and, in particular, removing rogue taxa significantly improved tree resolution and statistical support. Although our analyses rely on dense taxonomic sampling and substantial gene coverage, our results pinpoint the limited resolving power of Sanger sequencing‐era molecular phylogenetic datasets with respect to ancient, hyperdiverse radiations.

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.