Microbiota asociada a la glándula uropigial de aves; diversidad y funciones en escenarios de parasitismo y comunicación social

Abstract

Animals have evolved in a world dominated by microorganisms, engaging in relationships ranging from parasitism and commensalism to mutualism, where both the symbiotic microorganism and the host benefit from the interaction. These microorganisms often play important roles in the survival and reproductive success of animals, by facilitating or carrying out essential functions such as nutrient digestion, synthesizing vitamins, activating and maintaining the immune system, producing volatile compounds involved in animal communication, defending against pathogen infections, etc. Due to the benefits derived from acquiring and maintaining a suitable bacterial community, animal characteristics that allow the assembly of a bacterial community adapted to the environment should be under selection. Animals initiate the acquisition of their microbiota during the embryonic stage, continuing to acquire symbionts throughout their lives. Some bacterial symbionts are vertically transmitted from parents to offspring, typically during early life stages. However, acquiring symbionts directly from the environment in which animals develop (horizontal transmission), including individuals with whom they maintain physical contact (social environment) is also important for assembling an appropriate microbiota, since it allows the microbiota to adjust to the specific environmental characteristics in which the animal lives. One of the main benefits that animals obtain from the interaction with symbiotic microbiota, either within or on their body, is the defence against pathogenic microorganisms. Some bacteria produce antibiotic substances that impede the growth and development of potentially harmful microorganisms, thereby preventing infection in the individual or their offspring. In some animals, these bacteria thrive in specialized glands, such as the uropygial gland of birds. Specific compounds of the uropygial secretion have antimicrobial properties, and, recently, it was discovered in the Euorpean hoopoe (Upupa epops) that bacterial symbionts developing in their uropygial glands contribute, at least partially, to these antimicrobial properties. Over the past few decades, several bacterial strains have been isolated from the gland or its secretion in different bird species, which opens de possibility that the mutualistic interactions among gland-associated bacterial symbionts, producing antimicrobial substances, and their host might be more widespread than previously thought. Therefore, if the antimicrobial properties of these bacteria contribute to the host defences against pathogenic microorganisms, we would expect interspecific variations and an adjustment in the associated microbiota based on the risk of pathogenic infections experienced by their host. Symbiotic bacteria in animals also play an important role in both inter- and intraspecific communication, for instance, by producing volatile compounds perceived by receptors through smell. This is the case of several bird species, however, in the hoopoe the role of uropygial gland bacteria extends beyond potential olfactory communication; they also play a crucial role in visual communication between males and females. The colouration of the hoopoe's uropygial secretion depends on the bacterial community that develops within the gland, and females use this coloured secretion as a cosmetic substance to stain their eggs, thus signalling the quality of both themselves and their offspring to males. In general, cosmetic colouration mediated by the uropygial gland of birds has been studied mainly in contexts of sexual selection, with only few examples in contexts of parent-offspring communication. Nestlings of altricial bird species display brightly coloured mouths to their parents when begging, signalling their genetic quality or short-term needs. This colouration could be modified or enhanced if nestlings used the uropygial secretion, which can be transparent or coloured to the human eye, as a cosmetic substance to make up their mouths. If so, nestlings would convey not only information from the colouration of their mouths but also information from the colouration of their uropygial secretion. If in bird species beyond the hoopoe the colouration of the uropygial secretion also depended, partially, on the associated microbiota, these bacteria would play a crucial role in intraspecific visual communication, specifically between parents and offspring. The aims of this thesis are framed within these contexts of defence against pathogenic microorganisms and parent-offspring communication. We studied the possible role that bacteria might play in some known functions of the uropygial gland of birds. The thesis consists of two distinct parts. In the first part, through an interspecific study, we explore the hypothesis that uropygial gland bacteria contribute to defence against pathogens by producing antimicrobial compounds that complement the animal's own defences. In the second part of the thesis, through an experimental approach using the spotless starling (Sturnus unicolor) as a model species, we studied the hypothesis that bacteria, by producing or altering the uropygial secretion colouration, may be involved in intraspecific communication processes, specifically between parents and their offspring. Overall, the findings of this thesis demonstrate the importance of the bacterial community associated with the uropygial gland of birds and support the general hypothesis that these bacteria have a fundamental role in the functions previously suggested for this gland. This microbiota, on one hand, protect birds from infections caused by pathogenic microorganisms by producing substances with antimicrobial properties; and on the other hand, mediate in the intraspecific communication between parents and offspring by modifying the colouration of the secretion.