Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae.

Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genomic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families-genes directly mediating interactions with plant chemical defenses-underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many insect lineages are ancient (>150 million years ago (mya)), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several nonherbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza has among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant-binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on living plants (bitter or electrophilic phytotoxins) or their ancestral diet (fermenting plant volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight gene candidates that have also been linked to other dietary transitions in Drosophila.

Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae.

Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genetic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families - genes directly mediating interactions with plant chemical defenses - underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many lineages are ancient (>150 million years ago [mya]), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several non-herbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza have among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on plants (bitter or electrophilic phytotoxins) or their ancestral diet (yeast and fruit volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight strong gene candidates that have also been linked to other dietary transitions in Drosophila .

Ecological basis and genetic architecture of crypsis polymorphism in the desert clicker grasshopper (Ligurotettix coquilletti).

Color polymorphic species can offer exceptional insight into the ecology and genetics of adaptation. Although the genetic architecture of animal coloration is diverse, many color polymorphisms are associated with large structural variants and maintained by biotic interactions. Grasshoppers are notably polymorphic in both color and karyotype, which makes them excellent models for understanding the ecological drivers and genetic underpinnings of color variation. Banded and uniform morphs of the desert clicker grasshopper (Ligurotettix coquilletti) are found across the western deserts of North America. To address the hypothesis that predation maintains local color polymorphism and shapes regional crypsis variation, we surveyed morph frequencies and tested for covariation with two predation environments. Morphs coexisted at intermediate frequencies at most sites, consistent with local balancing selection. Morph frequencies covaried with the appearance of desert substrate-an environment used only by females-suggesting that ground-foraging predators are major agents of selection on crypsis. We next addressed the hypothesized link between morph variation and genome structure. To do so, we designed an approach for detecting inversions and indels using only RADseq data. The banded morph was perfectly correlated with a large putative indel. Remarkably, indel dominance differed among populations, a rare example of dominance evolution in nature.

Polyploidy in creosote bush (Larrea tridentata) shapes the biogeography of specialist herbivores.

AIM: Whole-genome duplication (polyploidy) can influence the biogeography and ecology of plants that differ in ploidy level (cytotype). Here, we address how two consequences of plant polyploidy (parapatry of cytotypes and altered species interactions) shape the biogeography of herbivorous insects. LOCATION: Warm deserts of North America. TAXA: Gall midges (Asphondylia auripila group, Diptera: Cecidomyiidae) that attack three parapatric cytotypes of creosote bush (Larrea tridentata, Zygophyllaceae). METHODS: We surveyed Asphondylia species diversity at 177 sites across a 2300-km extent. After noting a correspondence between the distributions of eight Asphondylia species and L. tridentata cytotypes, we fine-mapped Asphondylia species range limits with transects spanning cytotype contact zones. We then tested whether plant-insect interactions and/or abiotic factors explain this coincidence by (1) comparing attack rates and gall midge communities on alternative cytotypes in a narrow zone of sympatry and (2) using species distribution models (SDMs) to determine if climatically suitable habitat for each midge species extended beyond cytotype contact zones. RESULTS: The range limits of 6/17 Asphondylia species (including two novel putative species confirmed with COI sequencing) perfectly coincided with the contact zone of diploid and tetraploid L. tridentata. One midge species was restricted to diploid host plants while five were restricted to tetraploid and hexaploid host plants. Where diploid and tetraploid L. tridentata are sympatric, cytotype-restricted midge species more frequently attacked their typical host and Asphondylia community structure differed markedly between cytotypes. SDMs predicted that distributions of cytotype-restricted midge species were not constrained by climatic conditions near cytotype contact zones. MAIN CONCLUSIONS: Contact zones between plant cytotypes are dispersal barriers for many Asphondylia species due to plant-insect interactions. The distribution of L. tridentata cytotypes therefore shapes herbivore species ranges and herbivore community structure across North American deserts. Our results demonstrate that polyploidy in plants can affect the biogeography of ecological communities.

The Biogeography of Putative Microbial Antibiotic Production.

Understanding patterns in the distribution and abundance of functional traits across a landscape is of fundamental importance to ecology. Mapping these distributions is particularly challenging for species-rich groups with sparse trait measurement coverage, such as flowering plants, insects, and microorganisms. Here, we use likelihood-based character reconstruction to infer and analyze the spatial distribution of unmeasured traits. We apply this framework to a microbial dataset comprised of 11,732 ketosynthase alpha gene sequences extracted from 144 soil samples from three continents to document the spatial distribution of putative microbial polyketide antibiotic production. Antibiotic production is a key competitive strategy for soil microbial survival and performance. Additionally, novel antibiotic discovery is highly relevant to human health, making natural antibiotic production by soil microorganisms a major target for bioprospecting. Our comparison of trait-based biogeographical patterns to patterns based on taxonomy and phylogeny is relevant to our basic understanding of microbial biogeography as well as the pressing need for new antibiotics.

Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest.

The phyllosphere--the aerial surfaces of plants, including leaves--is a ubiquitous global habitat that harbors diverse bacterial communities. Phyllosphere bacterial communities have the potential to influence plant biogeography and ecosystem function through their influence on the fitness and function of their hosts, but the host attributes that drive community assembly in the phyllosphere are poorly understood. In this study we used high-throughput sequencing to quantify bacterial community structure on the leaves of 57 tree species in a neotropical forest in Panama. We tested for relationships between bacterial communities on tree leaves and the functional traits, taxonomy, and phylogeny of their plant hosts. Bacterial communities on tropical tree leaves were diverse; leaves from individual trees were host to more than 400 bacterial taxa. Bacterial communities in the phyllosphere were dominated by a core microbiome of taxa including Actinobacteria, Alpha-, Beta-, and Gammaproteobacteria, and Sphingobacteria. Host attributes including plant taxonomic identity, phylogeny, growth and mortality rates, wood density, leaf mass per area, and leaf nitrogen and phosphorous concentrations were correlated with bacterial community structure on leaves. The relative abundances of several bacterial taxa were correlated with suites of host plant traits related to major axes of plant trait variation, including the leaf economics spectrum and the wood density-growth/mortality tradeoff. These correlations between phyllosphere bacterial diversity and host growth, mortality, and function suggest that incorporating information on plant-microbe associations will improve our ability to understand plant functional biogeography and the drivers of variation in plant and ecosystem function.

Bacterial communities on classroom surfaces vary with human contact.

BACKGROUND: Humans can spend the majority of their time indoors, but little is known about the interactions between the human and built-environment microbiomes or the forces that drive microbial community assembly in the built environment. We sampled 16S rRNA genes from four different surface types throughout a university classroom to determine whether bacterial assemblages on each surface were best predicted by routine human interactions or by proximity to other surfaces within the classroom. We then analyzed our data with publicly-available datasets representing potential source environments. RESULTS: Bacterial assemblages from the four surface types, as well as individual taxa, were indicative of different source pools related to the type of human contact each surface routinely encounters. Spatial proximity to other surfaces in the classroom did not predict community composition. CONCLUSIONS: Our results indicate that human-associated microbial communities can be transferred to indoor surfaces following contact, and that such transmission is possible even when contact is indirect, but that proximity to other surfaces in the classroom does not influence community composition.

Architectural design drives the biogeography of indoor bacterial communities.

BACKGROUND: Architectural design has the potential to influence the microbiology of the built environment, with implications for human health and well-being, but the impact of design on the microbial biogeography of buildings remains poorly understood. In this study we combined microbiological data with information on the function, form, and organization of spaces from a classroom and office building to understand how design choices influence the biogeography of the built environment microbiome. RESULTS: Sequencing of the bacterial 16S gene from dust samples revealed that indoor bacterial communities were extremely diverse, containing more than 32,750 OTUs (operational taxonomic units, 97% sequence similarity cutoff), but most communities were dominated by Proteobacteria, Firmicutes, and Deinococci. Architectural design characteristics related to space type, building arrangement, human use and movement, and ventilation source had a large influence on the structure of bacterial communities. Restrooms contained bacterial communities that were highly distinct from all other rooms, and spaces with high human occupant diversity and a high degree of connectedness to other spaces via ventilation or human movement contained a distinct set of bacterial taxa when compared to spaces with low occupant diversity and low connectedness. Within offices, the source of ventilation air had the greatest effect on bacterial community structure. CONCLUSIONS: Our study indicates that humans have a guiding impact on the microbial biodiversity in buildings, both indirectly through the effects of architectural design on microbial community structure, and more directly through the effects of human occupancy and use patterns on the microbes found in different spaces and space types. The impact of design decisions in structuring the indoor microbiome offers the possibility to use ecological knowledge to shape our buildings in a way that will select for an indoor microbiome that promotes our health and well-being.

Microbial interactions and the ecology and evolution of Hawaiian Drosophilidae.

Adaptive radiations are characterized by an increased rate of speciation and expanded range of habitats and ecological niches exploited by those species. The Hawaiian Drosophilidae is a classic adaptive radiation; a single ancestral species colonized Hawaii approximately 25 million years ago and gave rise to two monophyletic lineages, the Hawaiian Drosophila and the genus Scaptomyza. The Hawaiian Drosophila are largely saprophagous and rely on approximately 40 endemic plant families and their associated microbes to complete development. Scaptomyza are even more diverse in host breadth. While many species of Scaptomyza utilize decomposing plant substrates, some species have evolved to become herbivores, parasites on spider egg masses, and exploit microbes on living plant tissue. Understanding the origin of the ecological diversity encompassed by these nearly 700 described species has been a challenge. The central role of microbes in drosophilid ecology suggests bacterial and fungal associates may have played a role in the diversification of the Hawaiian Drosophilidae. Here we synthesize recent ecological and microbial community data from the Hawaiian Drosophilidae to examine the forces that may have led to this adaptive radiation. We propose that the evolutionary success of the Hawaiian Drosophilidae is due to a combination of factors, including adaptation to novel ecological niches facilitated by microbes.

Significant changes in the skin microbiome mediated by the sport of roller derby.

Diverse bacterial communities live on and in human skin. These complex communities vary by skin location on the body, over time, between individuals, and between geographic regions. Culture-based studies have shown that human to human and human to surface contact mediates the dispersal of pathogens, yet little is currently known about the drivers of bacterial community assembly patterns on human skin. We hypothesized that participation in a sport involving skin to skin contact would result in detectable shifts in skin bacterial community composition. We conducted a study during a flat track roller derby tournament, and found that teammates shared distinct skin microbial communities before and after playing against another team, but that opposing teams' bacterial communities converged during the course of a roller derby bout. Our results are consistent with the hypothesis that the human skin microbiome shifts in composition during activities involving human to human contact, and that contact sports provide an ideal setting in which to evaluate dispersal of microorganisms between people.

Multigene phylogeny reveals eusociality evolved twice in vespid wasps.

Eusocial wasps of the family Vespidae are thought to have derived their social behavior from a common ancestor that had a rudimentary caste-containing social system. In support of this behavioral scenario, the leading phylogenetic hypothesis of Vespidae places the eusocial wasps (subfamilies Stenogastrinae, Polistinae, and Vespinae) as a derived monophyletic clade, thus implying a single origin of eusocial behavior. This perspective has shaped the investigation and interpretation of vespid social evolution for more than two decades. Here we report a phylogeny of Vespidae based on data from four nuclear gene fragments (18S and 28S ribosomal DNA, abdominal-A and RNA polymerase II) and representatives from all six extant subfamilies. In contrast to the current phylogenetic perspective, our results indicate two independent origins of vespid eusociality, once in the clade Polistinae+Vespinae and once in the Stenogastrinae. The stenogastrines appear as an early diverging clade distantly related to the vespines and polistines and thus evolved their distinctive form of social behavior from a different ancestor than that of Polistinae+Vespinae. These results support earlier views based on life history and behavior and have important implications for interpreting transitional stages in vespid social evolution.