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

2021 ◽  
Vol 224 (10) ◽  
Author(s):  
Jessica A. Cusick ◽  
Cara L. Wellman ◽  
Gregory E. Demas
Keyword(s):  
Gut Microbiome ◽  
Model Systems ◽  
Model Organisms ◽  
Comparative Approach ◽  
Wild Populations ◽  
Physiological Processes ◽  
Bidirectional Relationship ◽  
Microbiome Research ◽  
Host Behaviour ◽  
The Brain

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.

Pigeons as a model species for cognitive neuroscience

e-Neuroforum ◽  
2014 ◽  
Vol 20 (4) ◽  
Author(s):  
O. Güntürkün ◽  
M.C. Stüttgen ◽  
M. Manns
Keyword(s):  
Cognitive Neuroscience ◽  
Functional Organization ◽  
Model Systems ◽  
Model Organisms ◽  
Comparative Approach ◽  
Psychological Processes ◽  
Model Species ◽  
Comparative Neuroscience ◽  
Taxonomic Groups ◽  
The Brain

AbstractDeeper understanding of the neuronal basis of behavior and its evolution requires inves­tigation of model organisms taken from dif­ferent taxonomic groups. The merits of this comparative approach are highlighted by re­search on birds: while their cognitive capaci­ties have long been underestimated, research on avian model systems more recently has begun to provide central insights into the functional organization of the brain. In partic­ular, domesticated homing pigeons (Colum­ba livia) have been used as a model for the study of the psychological processes under­lying learning, memory, and choice behav­ior, and much of current animal learning the­ory is based on findings with pigeons. More­over, the vast amount of available behavior­al and anatomical data has rendered the pi­geon one of the key model species of behav­ioral and comparative neuroscience. This ar­ticle illustrates some insights gained from re­search with pigeons with applicability be­yond the class of aves.

The Gut Microbiome, Obesity, and Weight Control in Women’s Reproductive Health

2017 ◽  
Vol 39 (8) ◽  
pp. 1094-1119 ◽  
Author(s):  
K. Leigh Greathouse ◽  
Mary Ann Faucher ◽  
Marie Hastings-Tolsma
Keyword(s):  
Reproductive Health ◽  
Gut Microbiome ◽  
Weight Control ◽  
Energy Homeostasis ◽  
Energy Extraction ◽  
Human Gut ◽  
Microbiome Research ◽  
Prevalence Of Obesity ◽  
Offspring Health ◽  
The Brain

The microbes residing in the human gut, referred to as the microbiome, are intricately linked to energy homeostasis and subsequently obesity. Integral to the origins of obesity, the microbiome is believed to affect not only health of the human gut but also overall health. This microbiome–obesity association is mediated through the process of energy extraction, metabolism, and cross talk between the brain and the gut microbiome. Host exposures, including diet, that potentially modify genetic predisposition to obesity and affect weight management are reviewed. The higher prevalence of obesity among women and recent evidence linking obesity during pregnancy with offspring health make this topic particularly relevant. Current limitations in microbiome research to address obesity and future advances in this field are described. Applications of this science with respect to applied nursing and overall health care in general are included, with emphasis on the reproductive health of women and their offspring.

scholarly journals Evidence supporting the microbiota–gut–brain axis in a songbird

2020 ◽  
Vol 16 (11) ◽  
pp. 20200430
Author(s):  
Morgan C. Slevin ◽  
Jennifer L. Houtz ◽  
David J. Bradshaw ◽  
Rindy C. Anderson
Keyword(s):  
Gut Microbiome ◽  
Beta Diversity ◽  
Alpha Diversity ◽  
Cloacal Swab ◽  
Cognitive Tasks ◽  
Captive Population ◽  
Wild Populations ◽  
Alpha And Beta Diversity ◽  
Microbiome Research ◽  
Host Development

Recent research in mammals supports a link between cognitive ability and the gut microbiome, but little is known about this relationship in other taxa. In a captive population of 38 zebra finches ( Taeniopygia guttata ), we quantified performance on cognitive tasks measuring learning and memory. We sampled the gut microbiome via cloacal swab and quantified bacterial alpha and beta diversity. Performance on cognitive tasks related to beta diversity but not alpha diversity. We then identified differentially abundant genera influential in the beta diversity differences among cognitive performance categories. Though correlational, this study provides some of the first evidence of an avian microbiota–gut–brain axis, building foundations for future microbiome research in wild populations and during host development.

scholarly journals Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Gabrielle L. Davidson ◽  
Niamh Wiley ◽  
Amy C. Cooke ◽  
Crystal N. Johnson ◽  
Fiona Fouhy ◽  
...  
Keyword(s):  
Problem Solving ◽  
Gut Microbiota ◽  
Gut Microbiome ◽  
Parus Major ◽  
Behavioural Plasticity ◽  
Wild Populations ◽  
Problem Solve ◽  
Induced Changes ◽  
Host Behaviour ◽  
Problem Solving Task

AbstractThe microbial community in the gut is influenced by environmental factors, especially diet, which can moderate host behaviour through the microbiome-gut-brain axis. However, the ecological relevance of microbiome-mediated behavioural plasticity in wild animals is unknown. We presented wild-caught great tits (Parus major) with a problem-solving task and showed that performance was weakly associated with variation in the gut microbiome. We then manipulated the gut microbiome by feeding birds one of two diets that differed in their relative levels of fat, protein and fibre content: an insect diet (low content), or a seed diet (high content). Microbial communities were less diverse among individuals given the insect compared to those on the seed diet. Individuals were less likely to problem-solve after being given the insect diet, and the same microbiota metrics that were altered as a consequence of diet were also those that correlated with variation in problem solving performance. Although the effect on problem-solving behaviour could have been caused by motivational or nutritional differences between our treatments, our results nevertheless raise the possibility that dietary induced changes in the gut microbiota could be an important mechanism underlying individual behavioural plasticity in wild populations.

scholarly journals Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird

2019 ◽  
Author(s):  
Gabrielle L. Davidson ◽  
Niamh Wiley ◽  
Amy C. Cooke ◽  
Crystal N. Johnson ◽  
Fiona Fouhy ◽  
...  
Keyword(s):  
Problem Solving ◽  
Gut Microbiota ◽  
Gut Microbiome ◽  
Parus Major ◽  
Behavioural Plasticity ◽  
Wild Populations ◽  
Problem Solve ◽  
Induced Changes ◽  
Host Behaviour ◽  
Problem Solving Task

ABSTRACTThe microbial community in the gut is influenced by environmental factors, especially diet, which can moderate host behaviour through the microbiome-gut-brain axis. However, the ecological relevance of microbiome-mediated behavioural plasticity in wild animals is unknown. We presented wild-caught great tits (Parus major) with a problem-solving task and showed that performance was weakly associated with variation in the gut microbiome. We then manipulated the gut microbiome by feeding birds one of two diets that differed in their relative levels of fat, protein and fibre content: an insect diet (low content), or a seed diet (high content). Microbial communities were less diverse among individuals given the insect compared to those on the seed diet. Individuals were less likely to problem-solve after being given the insect diet, and the same microbiota metrics that were altered as a consequence of diet were also those that correlated with variation in problem solving performance. Although the effect on problem-solving behaviour could have been caused by motivational or nutritional differences between our treatments, our results nevertheless raise the possibility that dietary induced changes in the gut microbiota could be an important mechanism underlying individual behavioural plasticity in wild populations.

scholarly journals Host, microbiome, and complex space: applying population and landscape genetic approaches to gut microbiome research in wild populations

2022 ◽  
Author(s):  
Claire E Couch ◽  
Clinton W Epps
Keyword(s):  
Population Genetics ◽  
Gut Microbiome ◽  
Landscape Heterogeneity ◽  
Natural Populations ◽  
Host Population ◽  
Model Organisms ◽  
Wild Populations ◽  
Sequencing Technologies ◽  
Wild Host ◽  
Wide Range

Abstract In recent years, emerging sequencing technologies and computational tools have driven a tidal wave of research on host-associated microbiomes, particularly the gut microbiome. These studies demonstrate numerous connections between the gut microbiome and vital host functions, primarily in humans, model organisms, and domestic animals. As the adaptive importance of the gut microbiome becomes clearer, interest in studying the gut microbiomes of wild populations has increased, in part due to the potential for discovering conservation applications. The study of wildlife gut microbiomes holds many new challenges and opportunities due to the complex genetic, spatial, and environmental structure of wild host populations, and the potential for these factors to interact with the microbiome. The emerging picture of adaptive coevolution in host-microbiome relationships highlights the importance of understanding microbiome variation in the context of host population genetics and landscape heterogeneity across a wide range of host populations. We propose a conceptual framework for understanding wildlife gut microbiomes in relation to landscape variables and host population genetics, including the potential of approaches derived from landscape genetics. We use this framework to review current research, synthesize important trends, highlight implications for conservation, and recommend future directions for research. Specifically, we focus on how spatial structure and environmental variation interact with host population genetics and microbiome variation in natural populations, and what we can learn from how these patterns of covariation differ depending on host ecological and evolutionary traits.

scholarly journals Improving causality in microbiome research: can human genetic epidemiology help?

2020 ◽  
Vol 4 ◽  
pp. 199 ◽  
Author(s):  
Kaitlin H. Wade ◽  
Lindsay J. Hall
Keyword(s):  
Health Outcomes ◽  
Population Health ◽  
Gut Microbiome ◽  
Model Systems ◽  
Careful Examination ◽  
Research Review ◽  
Inherited Disease ◽  
Human Gut ◽  
Human Gut Microbiome ◽  
Microbiome Research

Evidence supports associations between human gut microbiome variation and multiple health outcomes and diseases. Despite compelling results from in vivo and in vitro models, few findings have been translated into an understanding of modifiable causal relationships. Furthermore, epidemiological studies have been unconvincing in their ability to offer causal evidence due to their observational nature, where confounding by lifestyle and behavioural factors, reverse causation and bias are important limitations. Whilst randomized controlled trials have made steps towards understanding the causal role played by the gut microbiome in disease, they are expensive and time-consuming. This evidence that has not been translated between model systems impedes opportunities for harnessing the gut microbiome for improving population health. Therefore, there is a need for alternative approaches to interrogate causality in the context of gut microbiome research. The integration of human genetics within population health sciences have proved successful in facilitating improved causal inference (e.g., with Mendelian randomization [MR] studies) and characterising inherited disease susceptibility. MR is an established method that employs human genetic variation as natural “proxies” for clinically relevant (and ideally modifiable) traits to improve causality in observational associations between those traits and health outcomes. Here, we focus and discuss the utility of MR within the context of human gut microbiome research, review studies that have used this method and consider the strengths, limitations and challenges facing this research. Specifically, we highlight the requirements for careful examination and interpretation of derived causal estimates and host (i.e., human) genetic effects themselves, triangulation across multiple study designs and inter-disciplinary collaborations. Meeting these requirements will help support or challenge causality of the role played by the gut microbiome on human health to develop new, targeted therapies to alleviate disease symptoms to ultimately improve lives and promote good health.

Synchronizing Our Clocks as We Age: The Influence of the Brain-Gut-Immune Axis on the Sleep-Wake Cycle Across the Lifespan

SLEEP ◽  
2021 ◽  
Author(s):  
Marissa Sgro ◽  
Zoe N Kodila ◽  
Rhys D Brady ◽  
Amy C Reichelt ◽  
Richelle Mychaisuk ◽  
...  
Keyword(s):  
Complex System ◽  
Immune System ◽  
Gut Microbiome ◽  
Neurological Development ◽  
Bidirectional Relationship ◽  
Integral Role ◽  
Vital Component ◽  
And Function ◽  
Communication Pathway ◽  
The Brain

Abstract The microbes that colonize the small and large intestines, known as the gut microbiome, play an integral role in optimal brain development and function. The gut microbiome is a vital component of the bi-directional communication pathway between the brain, immune system, and gut, also known as the brain-gut-immune axis. To date there has been minimal investigation into the implications of improper development of the gut microbiome and the brain-gut-immune axis on the sleep-wake cycle, particularly during sensitive periods of physical and neurological development, such as childhood, adolescence, and senescence. Therefore, this review will explore the current literature surrounding the overlapping developmental periods of the gut microbiome, brain, and immune system from birth through to senescence, while highlighting how the brain-gut-immune axis affects maturation and organisation of the sleep-wake cycle. We also examine how dysfunction to either the microbiome or the sleep-wake cycle negatively affects the bidirectional relationship between the brain and gut, and subsequently the overall health and functionality of this complex system. Additionally, this review integrates therapeutic studies to demonstrate when dietary manipulations, such as supplementation with probiotics and prebiotics, can modulate the gut microbiome to enhance health of the brain-gut-immune axis and optimize our sleep-wake cycle.

scholarly journals The relationship between the gut microbiome and host gene expression: a review

2020 ◽  
Author(s):  
Robert G. Nichols ◽  
Emily R. Davenport
Keyword(s):  
Gene Expression ◽  
Gut Microbiome ◽  
Host Gene ◽  
Model Organisms ◽  
Host Gene Expression ◽  
Immune Development ◽  
Physiological Processes ◽  
Host Signaling ◽  
Important Regulator ◽  
The Relationship

AbstractDespite the growing knowledge surrounding host–microbiome interactions, we are just beginning to understand how the gut microbiome influences—and is influenced by—host gene expression. Here, we review recent literature that intersects these two fields, summarizing themes across studies. Work in model organisms, human biopsies, and cell culture demonstrate that the gut microbiome is an important regulator of several host pathways relevant for disease, including immune development and energy metabolism, and vice versa. The gut microbiome remodels host chromatin, causes differential splicing, alters the epigenetic landscape, and directly interrupts host signaling cascades. Emerging techniques like single-cell RNA sequencing and organoid generation have the potential to refine our understanding of the relationship between the gut microbiome and host gene expression in the future. By intersecting microbiome and host gene expression, we gain a window into the physiological processes important for fostering the extensive cross-kingdom interactions and ultimately our health.

scholarly journals Improving causality in microbiome research: can human genetic epidemiology help?

2019 ◽  
Vol 4 ◽  
pp. 199 ◽  
Author(s):  
Kaitlin H. Wade ◽  
Lindsay J. Hall
Keyword(s):  
Health Outcomes ◽  
Population Health ◽  
Gut Microbiome ◽  
Model Systems ◽  
Careful Examination ◽  
Research Review ◽  
Inherited Disease ◽  
Human Gut ◽  
Human Gut Microbiome ◽  
Microbiome Research

Evidence supports associations between human gut microbiome variation and multiple health outcomes and diseases. Despite compelling results from in vivo and in vitro models, few findings have been translated into an understanding of modifiable causal relationships. Furthermore, epidemiological studies have been unconvincing in their ability to offer causal evidence due to their observational nature, where confounding by lifestyle and behavioural factors, reverse causation and bias are important limitations. Whilst randomized controlled trials have made steps towards understanding the causal role played by the gut microbiome in disease, they are expensive and time-consuming. This evidence that has not been translated between model systems impedes opportunities for harnessing the gut microbiome for improving population health. Therefore, there is a need for alternative approaches to interrogate causality in the context of gut microbiome research. The integration of human genetics within population health sciences have proved successful in facilitating improved causal inference (e.g., with Mendelian randomization [MR] studies) and characterising inherited disease susceptibility. MR is an established method that employs human genetic variation as natural “proxies” for clinically relevant (and ideally modifiable) traits to improve causality in observational associations between those traits and health outcomes. Here, we focus and discuss the utility of MR within the context of human gut microbiome research, review studies that have used this method and consider the strengths, limitations and challenges facing this research. Specifically, we highlight the requirements for careful examination and interpretation of derived causal estimates and host (i.e., human) genetic effects themselves, triangulation across multiple study designs and inter-disciplinary collaborations. Meeting these requirements will help support or challenge causality of the role played by the gut microbiome on human health to develop new, targeted therapies to alleviate disease symptoms to ultimately improve lives and promote good health.

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