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1. The call of the wild: using non-model systems to investigate microbiome–behaviour relationships

   https://doi.org/10.1242/jeb.224485  

   Cusick, Jessica A.; Wellman, Cara L.; Demas, Gregory E. (May 2021, Journal of Experimental Biology)

   null (Ed.)

   ABSTRACT On and within most sites across an animal's body live complex communities of microorganisms. These microorganisms perform a variety of important functions for their hosts, including communicating with the brain, immune system and endocrine axes to mediate physiological processes and affect individual behaviour. Microbiome research has primarily focused on the functions of the microbiome within the gastrointestinal tract (gut microbiome) using biomedically relevant laboratory species (i.e. model organisms). These studies have identified important connections between the gut microbiome and host immune, neuroendocrine and nervous systems, as well as how these connections, in turn, influence host behaviour and health. Recently, the field has expanded beyond traditional model systems as it has become apparent that the microbiome can drive differences in behaviour and diet, play a fundamental role in host fitness and influence community-scale dynamics in wild populations. In this Review, we highlight the value of conducting hypothesis-driven research in non-model organisms and the benefits of a comparative approach that assesses patterns across different species or taxa. Using social behaviour as an intellectual framework, we review the bidirectional relationship between the gut microbiome and host behaviour, and identify understudied mechanisms by which these effects may be mediated. 

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2. Connecting gut microbiomes and short chain fatty acids with the serotonergic system and behavior in Gallus gallus and other avian species

   https://doi.org/10.3389/fphys.2022.1035538  

   Jadhav, Vidya V.; Han, Jian; Fasina, Yewande; Harrison, Scott H. (November 2022, Frontiers in Physiology)

   Monika Proszkowiec-Weglarz, Agricultural Research (Ed.)

   The chicken gastrointestinal tract has a diverse microbial community. There is increasing evidence for how this gut microbiome affects specific molecular pathways and the overall physiology, nervous system and behavior of the chicken host organism due to a growing number of studies investigating conditions such as host diet, antibiotics, probiotics, and germ-free and germ-reduced models. Systems-level investigations have revealed a network of microbiome-related interactions between the gut and state of health and behavior in chickens and other animals. While some microbial symbionts are crucial for maintaining stability and normal host physiology, there can also be dysbiosis, disruptions to nutrient flow, and other outcomes of dysregulation and disease. Likewise, alteration of the gut microbiome is found for chickens exhibiting differences in feather pecking (FP) behavior and this alteration is suspected to be responsible for behavioral change. In chickens and other organisms, serotonin is a chief neuromodulator that links gut microbes to the host brain as microbes modulate the serotonin secreted by the host’s own intestinal enterochromaffin cells which can stimulate the central nervous system via the vagus nerve. A substantial part of the serotonergic network is conserved across birds and mammals. Broader investigations of multiple species and subsequent cross-comparisons may help to explore general functionality of this ancient system and its increasingly apparent central role in the gut-brain axis of vertebrates. Dysfunctional behavioral phenotypes from the serotonergic system moreover occur in both birds and mammals with, for example, FP in chickens and depression in humans. Recent studies of the intestine as a major site of serotonin synthesis have been identifying routes by which gut microbial metabolites regulate the chicken serotonergic system. This review in particular highlights the influence of gut microbial metabolite short chain fatty acids (SCFAs) on the serotonergic system. The role of SCFAs in physiological and brain disorders may be considerable because of their ability to cross intestinal as well as the blood-brain barriers, leading to influences on the serotonergic system via binding to receptors and epigenetic modulations. Examinations of these mechanisms may translate into a more general understanding of serotonergic system development within chickens and other avians. 

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3. Chronic stress and captivity alter the cloacal microbiome of a wild songbird

   https://doi.org/10.1242/jeb.243176  

   Madden, Anne A.; Oliverio, Angela M.; Kearns, Patrick J.; Henley, Jessica B.; Fierer, Noah; Starks, Philip T.; Wolfe, Benjamin E.; Romero, L. Michael; Lattin, Christine R. (April 2022, Journal of Experimental Biology)

   ABSTRACT There are complex interactions between an organism's microbiome and its response to stressors, often referred to as the ‘gut–brain axis’; however, the ecological relevance of this axis in wild animals remains poorly understood. Here, we used a chronic mild stress protocol to induce stress in wild-caught house sparrows (Passer domesticus), and compared microbial communities among stressed animals, those recovering from stress, captive controls (unstressed) and a group not brought into captivity. We assessed changes in microbial communities and abundance of shed microbes by culturing cloacal samples on multiple media to select for aerobic and anaerobic bacteria and fungi. We complemented this with cultivation-independent 16S and ITS rRNA gene amplification and sequencing, pairing these results with host physiological and immune metrics, including body mass change, relative spleen mass and plasma corticosterone concentrations. We found significant effects of stress and captivity on the house sparrow microbiomes, with stress leading to an increased relative abundance of endotoxin-producing bacteria – a possible mechanism for the hyperinflammatory response observed in captive avians. While we found evidence that the microbiome community partially recovers after stress cessation, animals may lose key taxa, and the abundance of endotoxin-producing bacteria persists. Our results suggest an overall link between chronic stress, host immune system and the microbiome, with the loss of potentially beneficial taxa (e.g. lactic acid bacteria), and an increase in endotoxin-producing bacteria due to stress and captivity. Ultimately, consideration of the host's microbiome may be useful when evaluating the impact of stressors on individual and population health. 

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4. The Effects of Social Experience on Host Gut Microbiome in Male Zebrafish ( Danio rerio )

   https://doi.org/10.1086/729377  

   Scott, Emily; Brewer, Michael S; Peralta, Ariane L; Issa, Fadi A (February 2024, The Biological Bulletin)

   Derby, C (Ed.)

   Although the gut and the brain vastly differ in physiological function, they have been interlinked in a variety of different neurological and behavioral disorders. The bacteria that comprise the gut microbiome communicate and influence the function of various physiological processes within the body, including nervous system function. However, the effects of social experience in the context of dominance and social stress on gut microbiome remain poorly understood. Here, we examined whether social experience impacts the host zebrafish (Danio rerio) gut microbiome. We studied how social dominance during the first 2 weeks of social interactions changed the composition of zebrafish gut microbiome by comparing gut bacterial composition, diversity, and relative abundance between socially dominant, submissive, social isolates and control group–housed communal fish. Using amplicon sequencing of the 16S rRNA gene, we report that social dominance significantly affects host gut bacterial community composition but not bacterial diversity. At the genus level, Aeromonas and unclassified Enterobacteriaceae relative abundance decreased in dominant individuals while commensal bacteria (e.g., Exiguobacterium and Cetobacterium) increased in relative abundance. Conversely, the relative abundance of Psychrobacter and Acinetobacter was increased in subordinates, isolates, and communal fish compared to dominant fish. The shift in commensal and pathogenic bacteria highlights the impact of social experience and the accompanying stress on gut microbiome, with potentially similar effects in other social organisms. 

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5. The buzz within: the role of the gut microbiome in honeybee social behavior

   https://doi.org/10.1242/jeb.246400  

   Nguyen, J B; Marshall, C W; Cook, C N (February 2024, Journal of Experimental Biology)

   ABSTRACT Gut symbionts influence the physiology and behavior of their host, but the extent to which these effects scale to social behaviors is an emerging area of research. The use of the western honeybee (Apis mellifera) as a model enables researchers to investigate the gut microbiome and behavior at several levels of social organization. Insight into gut microbial effects at the societal level is critical for our understanding of how involved microbial symbionts are in host biology. In this Commentary, we discuss recent findings in honeybee gut microbiome research and synthesize these with knowledge of the physiology and behavior of other model organisms to hypothesize how host–microbe interactions at the individual level could shape societal dynamics and evolution. 

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