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Animals and plants host diverse communities of microorganisms, and these microbiotas have been shown to influence host life history traits. Much has been said about the benefits that host-associated microbiotas bestow on the host. However, life history traits often demonstrate tradeoffs among one another. Raising Caenorhabditis elegans nematodes in compost microcosms emulating their natural environment, we examined how complex microbiotas affect host life history traits. We show that soil microbes usually increase the host development rate but decrease host resistance to heat stress, suggesting that interactions with complex microbiotas may mediate a tradeoff between host development and stress resistance. What element in these interactions is responsible for these effects is yet unknown, but experiments with live versus dead bacteria suggest that such effects may depend on bacterially provided signals.

Reproductive investment often comes at a cost to longevity, but the mechanisms that underlie these long-term effects are not well understood. In male vertebrates, elevated testosterone has been shown to increase reproductive success, but simultaneously to decrease survival. One factor that may contribute to or serve as a biomarker of these long-term effects of testosterone on longevity is telomeres, which are often positively related to lifespan and have been shown to shorten in response to reproduction. In this longitudinal study, we measured the effects of experimentally elevated testosterone on telomere shortening in free-living, male dark-eyed juncos (Junco hyemalis carolinensis), a system in which the experimental elevation of testosterone has previously been shown to increase reproductive success and reduce survival. We found a small, significant effect of testosterone treatment on telomeres, with testosterone-treated males exhibiting significantly greater telomere shortening with age than controls. These results are consistent with the hypothesis that increased telomere shortening may be a long-term cost of elevated testosterone exposure. As both testosterone and telomeres are conserved physiological mechanisms, our results suggest that their interaction may apply broadly to the long-term costs of reproduction in male vertebrates.

Symbiotic microbes that inhabit animal scent glands can produce volatile compounds used as chemical signals by the host animal. Though several studies have demonstrated correlations between scent gland bacterial community structure and host animal odour profiles, none have systematically demonstrated a causal relationship. In birds, volatile compounds in preen oil secreted by the uropygial gland serve as chemical cues and signals. Here, we tested whether manipulating the uropygial gland microbial community affects chemical profiles in the dark-eyed junco (Junco hyemalis). We found an effect of antibiotic treatment targeting the uropygial gland on both bacterial and volatile profiles. In a second experiment, we cultured bacteria from junco preen oil, and found that all of the cultivars produced at least one volatile compound common in junco preen oil, and that most cultivars produced multiple preen oil volatiles. In both experiments, we identified experimentally generated patterns in specific volatile compounds previously shown to predict junco reproductive success. Together, our data provide experimental support for the hypothesis that symbiotic bacteria produce behaviourally relevant volatile compounds within avian chemical cues and signals.

Culex pipiens, the endemic mosquito vector of West Nile virus in eastern North America, is responsible for maintenance of the virus in avian reservoir hosts, the most important of which appears to be the American robin. One reason for the greater involvement of robins is believed to be the feeding preference of Cx. pipiens, however, the basis of this preference is not understood. We tested the hypothesis that the species-specific chemical profile of avian uropygial gland secretions are used by Cx. pipiens as cues to locate birds and, therefore, may contribute to the observed feeding preferences. We used gas chromatography-mass spectrometry to identify the semi-volatile components of the uropygial gland secretions of American robins and two other common reservoir host species, the house sparrow and European starling. We found that the chemical composition of the robin secretions was different from those of the sparrows and starlings. Through behavioral choice trials conducted in a dual-port olfactometer, we also found that Cx. pipiens did not prefer the secretions of robins over the other two species. Surprisingly, however, we found that Cx pipiens were more often attracted to live starlings over robins and to the secretions of starlings over those of robins.

Chemical signals can provide useful information to potential mates and rivals. The production mechanisms of these signals are poorly understood in birds, despite emerging evidence that volatile compounds from preen oil may serve as chemosignals. Steroid hormones, including testosterone (T), may influence the production of these signals, yet variation in circulating T only partly accounts for this variation. We hypothesized that odor is a T-mediated signal of an individual's phenotype, regulated in part by androgen sensitivity in the uropygial gland. We quantified natural variation in chemosignals, T, uropygial gland androgen sensitivity, and aggressive behavior in dark-eyed juncos (Junco hyemalis). The interaction between circulating T and androgen receptor transcript abundance significantly correlated with volatile concentrations in male, but not female, preen oil. In both sexes, odorant variables correlated with aggressive response to an intruder. Our results suggest that preen oil volatiles could function as signals of aggressive intent, and, at least in males, may be regulated by local androgen receptor signaling in the uropygial gland. Because these behavioral and chemical traits have been linked with reproductive success, local regulation of androgen sensitivity in the periphery has the potential to be a target of selection in the evolution of avian olfactory signaling.

Chemical signaling is an underappreciated means of communication among birds, as may be the potential contributions of symbiotic microbes to animal chemical communication in general. The dark-eyed junco (Junco hyemalis) produces and detects volatile compounds that may be important in reproductive behavior. These compounds are found in preen oil secreted by the uropygial gland, and this gland supports diverse bacterial communities including genera known to produce some of these volatile compounds. We investigated the relative contributions of shared environments and genetic relatedness in shaping juncos' symbiotic bacterial communities, and investigated whether these bacterial communities underlie juncos' chemical signaling behavior. We sampled parents and nestlings at 9 junco nests during one breeding season at Mountain Lake Biological Station in Virginia, USA. From each individual, we collected swabs of the uropygial gland and the cloaca, preen oil, and a small blood sample for paternity testing. We characterized junco bacterial communities through 16S rRNA gene surveys and preen oil volatile compounds via gas chromatography-mass spectrometry. Nest membership and age class had the strongest influence on the structure of bacterial and volatile profiles. We compared father-offspring similarity based on paternity, and nestling similarity in nests containing full siblings and half siblings, and found that relatedness did not noticeably affect bacterial or volatile profiles. While we cannot rule out an influence of genetic relatedness on these profiles, it is clear that shared environments are more influential in shaping bacterial and volatile profiles among juncos. We did not find significant covariation between individual bacterial and volatile profiles. Possible explanations for this result include: (1) bacteria do not underlie volatile production; (2) ample redundancy in volatile production among bacterial types obscures covariation; or (3) the relationship is confounded by the fact that, unlike glands exclusively dedicated to chemical communication, uropygial glands have multiple functions, and symbiotic bacteria are hypothesized to contribute to each of these. Therefore, different bacteria may contribute to different phenotypes of the avian holobiont. Future work will include cultivation, metabolomic, genomic, and behavioral assay approaches to tease these scenarios apart.