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Animals live in a bacterial world, and detecting and exploring adaptations favouring mutualistic relationships with antibiotic‐producing bacteria as a strategy to fight pathogens are of prime importance for evolutionary ecologists. Uropygial secretion of European hoopoes (Upupa epops, Linnaeus) contains antimicrobials from mutualistic bacteria that may be used to prevent embryo infection. Here, we investigated the microscopic structure of hoopoe eggshells looking for special features favouring the adhesion of antimicrobial uropygial secretions. We impeded female access to the uropygial gland and compared microscopic characteristics of eggshells, bacterial loads of eggs and of uropygial secretion, and hatching success of experimental and control females. Then, we explored the link between microbiological characteristics of uropygial secretion and these of eggs of hoopoes, as well as possible fitness benefits. The microscopic study revealed special structures in hoopoes' eggshells (crypts). The experimental prevention of females' gland access demonstrated that crypts are filled with uropygial secretion and that symbiotic enterococci bacteria on the eggshells come, at least partially, from those in the female's uropygial gland. Moreover, the experiment resulted in a higher permeability of eggshells by several groups of bacteria and in elimination of the positive relationships detected for control nests between hatching success and density of symbiotic bacteria, either in the uropygial secretion of females or on the eggshell. The findings of specialized crypts on the eggshells of hoopoes, and of video‐recorded females smearing secretion containing symbiotic bacteria at a high density onto the eggshells strongly support a link between secretion and bacteria on eggs. Moreover, the detected associations between bacteria and hatching success suggest that crypts enhancing the adhesion of symbiont‐carrying uropygial secretion likely protect embryos against infections.

The study of associations between symbiotic bacterial communities of hosts and those of surrounding environments would help to understand how bacterial assemblages are acquired, and how they are transmitted from one to another location (i.e. symbiotic bacteria acquisition by hosts). Hoopoes (Upupa epops) smear their eggshells with uropygial secretion (oily secretion produced in their uropygial gland) that harbors antibiotic producing bacteria. Trying to elucidate a possible role of nest material and cloaca microbiota in determining the bacterial community of the uropygial gland and the eggshells of hoopoes, we characterized bacterial communities of nest material, cloaca, uropygial gland and eggshells by the ARISA fingerprinting. Further, by adding material with scarce bacteria and antimicrobial properties, we manipulated the bacterial community of nest material and thus tested experimentally its effects on the microbiomes of the uropygial secretion and of the eggshells. The experiment did not influence the microbiome of the uropygial secretion of females, but affected the community established on eggshells. This is the first experimental evidence indicating that nest material influences the bacterial community of the eggshells and, therefore, probability of embryo infection. Some of the bacterial strains detected in the secretion were also in the bacterial communities of the nest material and of cloaca, but their occurrence within nests was not associated, which suggests that bacterial environments of nest material and cloaca are not sources of symbiotic bacteria for the gland. These results do not support a role of nest environments of hoopoes as reservoirs of symbiotic bacteria. We discuss possible scenarios explaining bacterial acquisition by hoopoes that should be further explored.

The signalling hypothesis suggests that avian eggshell coloration is a sexually selected female signal advertising her quality to its male partner, thereby stimulating his provisioning rate. This hypothesis has been tested for structural eggshell pigments, but not for cosmetic colorations, such as that produced by the uropygial secretion on eggshells. During the breeding season, female hoopoes (Upupa epops) host in their uropygial glands symbiotic bacteria. Females actively smear the eggshells with their secretion, protecting embryos from pathogenic trans-shell infections and changing eggshell coloration. Because the colour of the secretions is related to their antimicrobial potential, cosmetic eggshell coloration may act as a cue or even as a post-mating sexually selected signal if it affects male provisioning rates. To experimentally test this hypothesis, we cross-fostered already-smeared clutches between hoopoe nests, and quantified male feeding behaviour to females before and after the experiment. This approach allows disentanglement of the effects of female quality and of egg coloration on male investment. In accordance with the hypothesis, males adjusted their provisioning rate to the eggshell cosmetic coloration. This is, to our knowledge, the first experimental demonstration that egg colour stained with uropygial secretion could act as a post-mating sexual signal of female quality to males.

Background Animals rely on symbiotic bacteria living within/on their tissues for multiple functions, while simultaneously needing to protect themselves via immune functions or other defenses from potentially pathogenic microorganisms that could invade those tissues. As a result, interactions with complex assemblages of bacteria have driven the evolution of host strategies to control established symbioses. One such strategy involves the development of organs specialized in maintaining associations with beneficial members of the microbial community — so-called symbiotic organs. These organs are characterized by compartmentalizing spaces where favorable conditions for the beneficial bacteria are promoted, while preventing colonization of other tissues. Although several model systems of symbiotic organs have been studied in animals, none have been recognized in non-aquatic vertebrates except for the intestinal crypts of mammals. Here, we propose that bird´s uropygial glands may be specialized symbiotic organs. Results We tested this hypothesis using the uropygial gland of the hoopoe ( Upupa epops ) as a model, which hosts a complex bacterial community that includes antimicrobial-producing symbionts. First, we examined whether the uropygial gland supports a specific symbiotic community, by comparing the microbiome composition of the uropygial secretions and eggshell surfaces in two European hoopoe populations. Additionally, using histological staining and fluorescence in situ hybridization, we looked for structural specializations for compartmentalization and bacterial targeting in the glands of nesting hoopoes in comparison to non-breeding individuals lacking the symbiosis. Results show that, in comparison with bacterial communities of the eggshells, those of the uropygial gland were more conserved between both populations. Moreover, uropygial glands of nesting hoopoes were strictly compartmentalized by a special tissue, properties that are absent in the non-breeding individuals lacking the symbiosis. Finally, bacteria were organized within the organ, suggesting the existence of special physical niches to promote specialized mutualistic symbionts. Conclusions All evidence supports that the hoopoe uropygial gland is a specialized symbiotic organ for bacterial cultivation, paving the way for new insights into vertebrates’ exocrine glands’ role in microbial symbiosis. Clinical trial number Not applicable.

Molecular methods have revealed that symbiotic systems involving bacteria are mostly based on whole bacterial communities. Bacterial diversity in hoopoe uropygial gland secretion is known to be mainly composed of certain strains of enterococci, but this conclusion is based solely on culture-dependent techniques. This study, by using culture-independent techniques (based on the 16S rDNA and the ribosomal intergenic spacer region) shows that the bacterial community in the uropygial gland secretion is more complex than previously thought and its composition is affected by the living conditions of the bird. Besides the known enterococci, the uropygial gland hosts other facultative anaerobic species and several obligated anaerobic species (mostly clostridia). The bacterial assemblage of this community was largely invariable among study individuals, although differences were detected between captive and wild female hoopoes, with some strains showing significantly higher prevalence in wild birds. These results alter previous views on the hoopoe-bacteria symbiosis and open a new window to further explore this system, delving into the possible sources of symbiotic bacteria (e.g. nest environments, digestive tract, winter quarters) or the possible functions of different bacterial groups in different contexts of parasitism or predation of their hoopoe host.

Symbiotic microorganisms may be directly transferred from parents to offspring or acquired from a particular environment that animals may be able to select. If benefits for hosts vary among microbial strains, natural selection may favour hosts holding the most beneficial one. Enterococci symbionts living in the hoopoe (Upupa epops) uropygial gland are able to synthesise bacteriocins (antimicrobial peptides that inhibit the growth of competitor bacteria). We explored variability in genetic profile (through RAPD-PCR analyses) and antimicrobial properties (by performing antagonistic tests against ten bacterial indicator strains) of the different isolates obtained from the uropygial glands of hoopoe females and nestlings. We found that the genetic profile of bacterial isolates was related to antimicrobial activity, as well as to individual host identity and the nest from which samples were obtained. This association suggest that variation in the inhibitory capacity of Enterococci symbionts should be under selection.

The microbiome of the uropygial gland and integuments where birds spread the uropygial secretion may play crucial roles for their hosts, but it has been poorly studied, especially in wild species. Exploring bacterial communities associated with the uropygial secretion of birds is particularly interesting in species under strong selection pressures due to pathogenic infection. Here, by high‐throughput 16S rRNA amplicon sequencing, we characterized and compared the bacterial communities of the uropygial gland surface of three African hornbill species (Family Bucerotidae), as well as the bill and feathers of females from two of these species and the nestlings of the other one. In accordance with previous knowledge of avian microbiomes, we expected to find differences associated with species identity, age and the sampled integument. Overall, we found that: 1) the microbiome was similar among species, 2) but there were slight differences associated with the sampled body regions. Moreover, 3) we observed no consistent variation in the microbiota with age, and 4) females and nestlings sharing a nest harboured more similar gland surface microbiota compared to females and nestlings that did not share a nest. These species often reuse nest cavities, sealing them with a plug made from diverse material. Once sealed, they remain enclosed in the nest for a long period. This behaviour opens the possibility that the nest environment is key shaping the microbiota of these species and might serve as a reservoir of the sampled bacterial communities. Moreover, behavioural mechanisms such as preening may contribute to the transmission of bacteria from the uropygial gland to other body regions, enhancing bacterial similarities. This study contributes to our understanding of the role of the nest environment in structuring bacterial communities in wild birds and provides the first thorough characterization of the microbiome inhabiting different body integuments of southern African hornbills.

The European hoopoe ( Upupa epops ) conforms a paradigmatic example of animals cultivating bacteria in their uropygial gland that protect them against pathogenic infections. We here explore the hypothesis that enterococci are the responsible bacteria of such beneficial effect. We did so by comparing the antimicrobial activity against three indicator bacteria of colonies isolated from cultures of enterococci and mesophilic bacteria from the uropygial skin or secretion of nestlings, brooding or non-brooding females, and males of the subspecies longirostris in Hainan (China). In accordance with the hypothesis, enterococci isolated from nesting birds are more active than those from non-nesting birds. Moreover, enterococci from the uropygial secretion were more active than those isolated from the skin or than mesophilic bacteria isolates. These results therefore support the hypothesis that, during the nesting phase, hoopoe females and nestlings cultivate enterococci in their uropygial gland with relatively high antimicrobial activity.

Animals frequently use metabolites produced by symbiotic bacteria as agents against pathogens and parasites. Secretions from the preen gland of birds are used for this purpose, although its chemicals apparently are produced by the birds themselves. European hoopoes Upupa epops and green woodhoopoes Phoeniculus purpureus harbour symbiotic bacteria in the uropygial gland that might be partly responsible for the chemical composition of secretions. Here we investigate the antimicrobial activity of the volatile fraction of chemicals in hoopoe preen secretions, and, by means of experimental antibiotic injections, test whether symbiotic bacteria living within the uropygial gland are responsible for their production. Hoopoes produce two different kinds of secretions that differ drastically in their chemical composition. While the malodorous dark secretions produced by nestlings included a complex mix of volatiles, these chemicals did not appear in white secretions produced by non-nesting birds. All volatiles detected showed strong antibacterial activity, and a mixture of the chemicals at the concentrations measured in nestling glands inhibited the growth of all bacterial strains assayed. We found support for the hypothesized role of bacteria in the production of such antimicrobial chemicals because experimental clearance of bacteria from glands of nestlings with antibiotics resulted in secretions without most of the volatiles detected in control individuals. Thus, the presence of symbiotic bacteria in the uropygial gland provides hoopoes with potent antimicrobials for topical use.

Background Animal bacterial symbionts are established early in life, either through vertical transmission and/or by horizontal transmission from both the physical and the social environment, such as direct contact with con- or heterospecifics. The social environment particularly can influence the acquisition of both mutualistic and pathogenic bacteria, with consequences for the stability of symbiotic communities. However, segregating the effects of the shared physical environment from those of the social interactions is challenging, limiting our current knowledge on the role of the social environment in structuring bacterial communities in wild animals. Here, we take advantage of the avian brood-parasite system of Eurasian magpies ( Pica pica ) and great spotted cuckoos ( Clamator glandarius ) to explore how the interspecific social environment (magpie nestlings developing with or without heterospecifics) affects bacterial communities on uropygial gland skin. Results We demonstrated interspecific differences in bacterial community compositions in members of the two species when growing up in monospecific nests. However, the bacterial community of magpies in heterospecific nests was richer, more diverse, and more similar to their cuckoo nest-mates than when growing up in monospecific nests. These patterns were alike for the subset of microbes that could be considered core, but when looking at the subset of potentially pathogenic bacterial genera, cuckoo presence reduced the relative abundance of potentially pathogenic bacterial genera on magpies. Conclusions Our findings highlight the role of social interactions in shaping the assembly of the avian skin bacterial communities during the nestling period, as exemplified in a brood parasite—host system.