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Hammer, T. J.

Publications and source records attributed to Hammer, T. J..

6 recordsLinked to original sources

Sparse gut microbiomes in solitary bees and wasps

Bees and wasps are ecologically vital, but many species are declining due to anthropogenic stressors. Social bees harbour host-specific and dense gut microbiomes that affect their resilience to stress. However, there are tens of thousands of other bee and wasp species that vary in sociality and diet (including pollen-feeding and predatory guilds), traits known to influence host-microbe symbioses. The role of gut microbes in the biology of these species is largely unknown. Here, we measured the composition and absolute abundance of bacterial communities in adult abdomens across 61 genera and 14 families of field-collected bees, predatory wasps, and pollen wasps. We found that solitary bees and both wasp guilds harbor distinct bacterial taxa and lower bacterial abundances as compared with social bees. Bacterial abundances also varied extensively among and within genera of solitary bees, with little variation explained by body size, diet breadth, or nesting ecology. Further, microbiome composition was only weakly differentiated among solitary bees and the two wasp groups, even comparing herbivorous (pollen-feeding) and carnivorous taxa. We suggest that the sparse and somewhat stochastic microbiomes of solitary bees and wasps reflect weak host dependence on microbially mediated functions, a trait that may influence their responses to environmental change.

ecology↗

Pervasive and dynamic gut dysbiosis in wild bumble bees is linked to the host life cycle

Stressors can shift the microbiome into an altered, "dysbiotic" state that reduces host fitness. While well-studied in humans and laboratory models, the prevalence, predictability, and drivers of dysbiosis in wildlife remain unclear. We addressed these questions by monitoring gut microbiomes of wild bumble bees in Southern California, focusing on Bombus vosnesenskii, a major pollinator in western North America. More than a third of all B. vosnesenskii bees exhibited dysbiosis, when defined as a >50% replacement of host-specialized core bacteria by environmental bacteria. This replacement covaried with increased alpha and beta diversity, an enrichment of oxygen-tolerant taxa, and pathogen infection--all common hallmarks of dysbiosis in other hosts. Other co-occurring Bombus, including two at-risk species, also exhibited dysbiosis. In B. vosnesenskii, dysbiosis was not correlated with certain stressors, such as heat or resource limitation, although other, unmeasured stressors cannot be ruled out. We next examined how dysbiosis varied over two years of sampling. In the first year, dysbiosis emerged only late in the season, when bumble bee colonies normally reproduce and then senesce. Two years later, following an intervening year with historic rainfall and elevated resources, dysbiosis was entrenched throughout the season. These findings show that dysbiosis is both pervasive and highly dynamic in wild bumble bees. The dynamics coincide with host life cycle transitions and environmental change, but the underlying causality remains uncertain. Given that dysbiosis may harm host health, we argue that long-term microbiome monitoring should be considered both for bumble bees and for other wildlife of conservation concern.

microbiology↗

Microbiome assembly and maintenance across the lifespan of bumble bee workers

How a hosts microbiome changes over its lifespan can influence development and aging. As these temporal patterns have only been described in detail for humans and a handful of other hosts, an important next step is to compare microbiome dynamics across a broader array of host-microbe symbioses, and to investigate how and why they vary. Here we characterize the temporal dynamics and stability of the bumblebee worker gut microbiome. Bumblebees are a useful symbiosis model given their relatively well-understood life history and simple, host-specific gut bacterial communities. Furthermore, microbial dynamics may influence bumblebee health and pollination services. We combined high-temporal-resolution sampling with 16S rRNA gene sequencing, quantitative PCR, and shotgun metagenomics to characterize gut microbiomes over the adult lifespan of Bombus impatiens workers. To understand how hosts may control (or lose control of) the gut microbiome as they age, we also sequenced hindgut transcriptomes. We found that, at the community level, microbiome assembly is highly predictable and similar to patterns of primary succession observed in the human gut. At the same time, partitioning of strain-level bacterial variants among colonies suggests stochastic colonization events similar to those observed in flies and nematodes. We also find strong differences in temporal dynamics among symbiont species, suggesting ecological differences among microbiome members in colonization and persistence. Finally, we show that both the gut microbiome and host transcriptome--including expression of key immunity genes--stabilize, as opposed to senesce, with age. We suggest that in highly social groups such as bumblebees, maintenance of both microbiomes and immunity contribute to the inclusive fitness of workers, and thus remain under selection even in old age. Our findings provide a foundation for exploring the mechanisms and functional outcomes of bee microbiome succession, and for comparative analyses with other host-microbe symbioses.

microbiology↗

Thermal niches of specialized gut symbionts: the case of social bees

Responses to climate change are particularly complicated in species that engage in symbioses, as the niche of one partner may be modified by that of the other. We explored thermal traits in gut symbionts of honeybees and bumblebees, which are vulnerable to rising temperatures. In vitro assays of symbiont strains isolated from 16 host species revealed variation in thermal niches. Strains from bumblebees tended to be less heat-tolerant than those from honeybees, possibly due to bumblebees maintaining cooler nests or inhabiting cooler climates. Overall however, bee symbionts grew at temperatures up to 44 {degrees}C and withstood temperatures up to 52 {degrees}C, at or above the upper thermal limits of their hosts. While heat-tolerant, most strains of the symbiont Snodgrassella grew relatively slowly below 35 {degrees}C, perhaps because of adaptation to the elevated body temperatures that bees maintain through thermoregulation. In a gnotobiotic bumblebee experiment, Snodgrassella was unable to consistently colonize bees reared below 35 {degrees}C under conditions that limit thermoregulation. Thus, host thermoregulatory behavior appears important in creating a warm microenvironment for symbiont establishment. Bee-microbiome-temperature interactions could affect host health and pollination services, and inform research on the thermal biology of other specialized gut symbionts, such as those of humans.

microbiology↗

Pollen-feeding Heliconius butterflies host distinctive adult-stage microbiomes

Lepidoptera (butterflies and moths) are diverse and ecologically important, yet we know little about how they interact with microbes as adults. Due to metamorphosis, the form and function of their adult-stage microbiomes might be very different from microbiomes in the larval stage (caterpillars). We studied adult-stage microbiomes of Heliconius and closely related passion-vine butterflies (Heliconiini), which are an important model system in evolutionary biology. To characterize the structure and dynamics of heliconiine microbiomes, we used field collections of wild butterflies, 16S rRNA gene sequencing, quantitative PCR, and shotgun metagenomics. We found that Heliconius harbor simple and abundant bacterial communities that are moderately consistent among conspecific individuals and over time. Heliconiine microbiomes also exhibited a strong signal of host phylogeny, with a major distinction between Heliconius and other butterflies. These patterns were largely driven by differing relative abundances of bacterial phylotypes shared among host species and genera, as opposed to the presence or absence of host-specific phylotypes. We suggest that phylogenetic structure in heliconiine microbiomes arises from conserved host traits that differentially filter microbes from the environment. While the relative importance of different traits remains unclear, our data indicate that pollen-feeding (unique to Heliconius) is not a primary driver. Using shotgun metagenomics, we also discovered trypanosomatids and microsporidia to be prevalent in butterfly guts, raising the possibility of antagonistic interactions between eukaryotic parasites and co-localized gut bacteria. Our discovery of characteristic and phylogenetically structured microbiomes provides a foundation for tests of adult-stage microbiome function, a poorly understood aspect of lepidopteran biology. ImportanceMany insects host microbiomes with important ecological functions. However, the prevalence of this phenomenon is unclear, because in many insect taxa microbiomes have only been studied in part of the life cycle, if at all. A prominent example is the butterflies and moths, in which the composition and functional role of adult-stage microbiomes are largely unknown. We comprehensively characterized microbiomes in adult passion-vine butterflies. Butterfly-associated bacterial communities are generally abundant in guts, consistent within populations, and composed of taxa widely shared among hosts. More closely related butterflies harbor more similar microbiomes, with the most dramatic shift in microbiome composition occurring in tandem with a suite of ecological and life history traits unique to the genus Heliconius. Butterflies are also frequently infected with previously undescribed eukaryotic parasites, which may interact with bacteria in important ways. These findings advance our understanding of butterfly biology and of insect-microbe interactions generally.

ecology↗

Caterpillars lack a resident gut microbiome

Many animals are inhabited by microbial symbionts that influence their hosts development, physiology, ecological interactions, and evolutionary diversification. However, firm evidence for the existence and functional importance of resident microbiomes in larval Lepidoptera (caterpillars) is lacking, despite the fact that these insects are enormously diverse, major agricultural pests, and dominant herbivores in many ecosystems. Using 16S rRNA gene sequencing and quantitative PCR, we characterized the gut microbiomes of wild leaf-feeding caterpillars in the United States and Costa Rica, representing 124 species from 16 families. Compared with other insects and vertebrates assayed using the same methods, the microbes we detected in caterpillar guts were unusually low-density and highly variable among individuals. Furthermore, the abundance and composition of leaf-associated microbes were reflected in the feces of caterpillars consuming the same plants. Thus, microbes ingested with food are present (though possibly dead or dormant) in the caterpillar gut, but host-specific, resident symbionts are largely absent. To test whether transient microbes might still contribute to feeding and development, we conducted an experiment on field-collected caterpillars of the model species Manduca sexta. Antibiotic suppression of gut bacterial activity did not significantly affect caterpillar weight gain, development, or survival. The high pH, simple gut structure, and fast transit times that typify caterpillar digestive physiology may prevent microbial colonization. Moreover, host-encoded digestive and detoxification mechanisms likely render microbes unnecessary for caterpillar herbivory. Caterpillars illustrate the potential ecological and evolutionary benefits of independence from symbionts, a lifestyle which may be widespread among animals.

ecology↗