Microbes, herbivory and the evolution of social behavior

doi:10.1016/0022-5193(84)90016-X

Journal of Theoretical Biology

Volume 106, Issue 2, 21 January 1984, Pages 157-169

https://doi.org/10.1016/0022-5193(84)90016-X Get rights and content

Abstract

Herbivorous animals that digest plant structural tissues almost invariably depend on the fermentative activity of symbiotic populations of microbes, housed in the digestive tract, to degrade plant fiber. The evolution of microbial fermentation systems entails an intricate coevolution among microbe species, as well as between microbes and herbivores. Beyond some level of biochemical specialization, fermentative microflora cannot survive outside of the host's body, and can only be transferred among herbivores by close contact. Yet in order actually to coevolve with the herbivore species, the microbe populations must be transmitted from one generation of herbivore to the next. In order to evolve the most effective system for utilizing plant materials for food, i.e. dependence on a microbial fermentation system, herbivores must concurrently evolve behavioral adaptations that ensure contact between generations. The evolution of social systems in a variety of animals, from termites to dinosaurs, may be originally associated with their herbivorous habits.

References (50)

K. Bjorndal
Comp. Biochem. Physiol
(1979)
W.C. Gasaway
Comp. Biochem. Physiol
(1976)
W.D. Hamilton
J. theor. Biol
(1971)
R.H. McBee
Am. J. Clin. Nutr
(1970)
R.D. Alexander
A. Rev. Ecol. Syst
(1974)
R.M. Alexander
Nature
(1976)
R.T. Bakker
Discovery (Peabody Museum, Yale)
(1968)
T. Bauchop
The Ecology of Arboreal Folivores
T. Bauchop et al.
Science
(1968)
G.M. Burghardt
Am. Zool
(1977)

G.M. Burghardt et al.

Science

(1977)

T.J. Case

Paleobiology

(1978)

L.R. Cleveland

Quart. Rev. Biol

(1926)

L.R. Cleveland

Anat. Rec

(1930)

L.R. Cleveland et al.

Mem. Am. Acad. Arts Sci

(1934)

M.W. Demment et al.

Body Size, Digestive Capacity and Feeding Strategies of Herbivores

(1982)

J.O. Farlow

Ecology

(1976)

K. Francis-Smith et al.

Equine Vet. J

(1977)

V. Geist

Am. Zool

(1974)

J.R. Gosz et al.

Sci. Am

(1978)

H.W. Greene et al.

J. Herpetol

(1978)

J.R. Horner et al.

Nature

(1979)

N. Hotton

A Cold Look at the Warm-blooded Dinosaurs

R.E. Hungate

The Rumen and its Microbes

(1966)

Cited by (51)

Microbial transmission in the social microbiome and host health and disease
2024, Cell
Although social interactions are known to drive pathogen transmission, the contributions of socially transmissible host-associated mutualists and commensals to host health and disease remain poorly explored. We use the concept of the social microbiome—the microbial metacommunity of a social network of hosts—to analyze the implications of social microbial transmission for host health and disease. We investigate the contributions of socially transmissible microbes to both eco-evolutionary microbiome community processes (colonization resistance, the evolution of virulence, and reactions to ecological disturbance) and microbial transmission-based processes (transmission of microbes with metabolic and immune effects, inter-specific transmission, transmission of antibiotic-resistant microbes, and transmission of viruses). We consider the implications of social microbial transmission for communicable and non-communicable diseases and evaluate the importance of a socially transmissible component underlying canonically non-communicable diseases. The social transmission of mutualists and commensals may play a significant, under-appreciated role in the social determinants of health and may act as a hidden force in social evolution.
Germ-Free Animals: A Key Tool in Unraveling How the Microbiota Affects the Brain and Behavior
2024, The Gut-Brain Axis, Second Edition
Numerous studies have implicated the gut microbiota in the development, function, and maintenance of brain health and behavior. Indeed, research utilizing germ-free animals (animals raised devoid of all microorganisms) has been instrumental in providing evidence supporting a role for gut microbes in gut–brain axis communication. Key findings have highlighted the role of the gut microbiota in a multitude of neurophysiological processes including neurogenesis, myelination, blood–brain barrier permeability, neuroplasticity, neurotransmission, microglial activation, and neuroinflammation. Further, the molecular mechanisms underlying germ-free behavior are being elucidated and implicate gut microbes in a myriad of complex behaviors including stress responsivity, anxiety-like behavior, sociability, and cognition. Though the germ-free mouse has been the model employed by most studies linking the gut microbiota to the brain, alternative models such as zebrafish, Drosophila, Caenorhabditis elegans, and the pig are also emerging, further advancing our mechanistic understanding of microbiota–gut–brain communication. The principal advantage of the germ-free model is in proof-of-principle studies, whereby researchers can selectively introduce a specific bacterium or consortium and investigate its mechanistic underpinnings during specific windows throughout the host's lifespan. However, a germ-free upbringing significantly influences neurodevelopmental outcomes that may deem them unsuitable for certain investigations. Further, limited translatability to humans is another key consideration in the use of germ-free models, highlighting the need for alternative and complementary strategies. Increasing our understanding of the impact of the gut microbiota on brain health and behavior using a variety of approaches will enable the development of novel therapeutics targeting disorders associated with perturbed microbiota–gut–brain axis signaling.
Leveraging non-human primates for exploring the social transmission of microbes
2019, Current Opinion in Microbiology
Citation Excerpt :
Therefore, mechanisms to maintain microbial diversity are likely under selection pressure. Because of the potential benefits of horizontal microbial transmission, suites of social behaviors may have evolved to buffer against transmission of pathogenic microbes while facilitating sharing of beneficial ones [2,14,17,18]. Though limited empirical data exist to support this hypothesis, many primate behaviors could serve these functions.
Host social interactions can provide multiple complex pathways for microbial transmission. Here, we suggest non-human primates as models to study the social transmission of commensal or mutualistic microbes due to their high sociality, wide range of group compositions and dominance structures, and diverse group interactions. Microbial sharing from social interactions can positively impact host health by promoting microbial diversity and influencing immunity. Microbes may also drive their own transmission by shaping host behavior, which could lead to fitness benefits for both microbes and hosts. Variation in patterns of social interactions at both the individual and group scale make non-human primates an ideal system to explore the relationship between social behavior, microbial sharing, and their impact on host health and evolution.
The Neuroendocrinology of the Microbiota-Gut-Brain Axis: A Behavioural Perspective
2018, Frontiers in Neuroendocrinology
Citation Excerpt :
Sociability is a key aspect of mammals’ lifespan. In the last decades, numerous studies have been focusing on how social interactions take place across different species and some studies have suggested that the endosymbiotic microbes shared in group living have influenced the evolution of social behaviour (Lombardo, 2008; Montiel-Castro et al., 2013; Troyer, 1984). The microbiota has been linked to social status across a variety of species including Drosophila (Lize et al., 2014; Venu et al., 2014), bumblebees (Koch and Schmid-Hempel, 2011), hyenas (Theis et al., 2013), non-human primates in the wild (Tung et al., 2015) and rodents.
The human gut harbours trillions of symbiotic bacteria that play a key role in programming different aspects of host physiology in health and disease. These intestinal microbes are also key components of the gut-brain axis, the bidirectional communication pathway between the gut and the central nervous system (CNS). In addition, the CNS is closely interconnected with the endocrine system to regulate many physiological processes. An expanding body of evidence is supporting the notion that gut microbiota modifications and/or manipulations may also play a crucial role in the manifestation of specific behavioural responses regulated by neuroendocrine pathways. In this review, we will focus on how the intestinal microorganisms interact with elements of the host neuroendocrine system to modify behaviours relevant to stress, eating behaviour, sexual behaviour, social behaviour, cognition and addiction.
The neuropharmacology of butyrate: The bread and butter of the microbiota-gut-brain axis?
2016, Neurochemistry International
Citation Excerpt :
Moreover, a study in Drosophila could demonstrate that SCFAs decreased longevity through a connection between metabolism and histone acetylation (Peleg et al., 2016). Due to their intimate relationship with the host, microbes have been suggested to play important roles in establishing host social behaviours and particularly the evolution and development of mammalian social group living by mutual benefit to the fitness of both host and microbes (Lombardo, 2008; Montiel-Castro et al., 2013, 2014; Stilling et al., 2014a; Troyer, 1984). However, it is not entirely clear how communication between individuals of a certain host species can be influenced by the presence and activity of bacteria.
Several lines of evidence suggest that brain function and behaviour are influenced by microbial metabolites. Key products of the microbiota are short-chain fatty acids (SCFAs), including butyric acid. Butyrate is a functionally versatile molecule that is produced in the mammalian gut by fermentation of dietary fibre and is enriched in butter and other dairy products. Butyrate along with other fermentation-derived SCFAs (e.g. acetate, propionate) and the structurally related ketone bodies (e.g. acetoacetate and d-β-hydroxybutyrate) show promising effects in various diseases including obesity, diabetes, inflammatory (bowel) diseases, and colorectal cancer as well as neurological disorders. Indeed, it is clear that host energy metabolism and immune functions critically depend on butyrate as a potent regulator, highlighting butyrate as a key mediator of host-microbe crosstalk. In addition to specific receptors (GPR43/FFAR2; GPR41/FFAR3; GPR109a/HCAR2) and transporters (MCT1/SLC16A1; SMCT1/SLC5A8), its effects are mediated by utilisation as an energy source via the β-oxidation pathway and as an inhibitor of histone deacetylases (HDACs), promoting histone acetylation and stimulation of gene expression in host cells. The latter has also led to the use of butyrate as an experimental drug in models for neurological disorders ranging from depression to neurodegenerative diseases and cognitive impairment.
Here we provide a critical review of the literature on butyrate and its effects on multiple aspects of host physiology with a focus on brain function and behaviour. We find fundamental differences in natural butyrate at physiological concentrations and its use as a neuropharmacological agent at rather high, supraphysiological doses in brain research. Finally, we hypothesise that butyrate and other volatile SCFAs produced by microbes may be involved in regulating the impact of the microbiome on behaviour including social communication.
Gut mutualists can persist in host populations despite low fidelity of vertical transmission
2022, Evolutionary Human Sciences
The shame system appears to be natural selection's solution to the adaptive problem of information-triggered reputational damage. Over evolutionary time, this problem would have led to a coordinated set of adaptations – the shame system – designed to minimise the spread of negative information about the self and the likelihood and costs of being socially devalued by others. This information threat theory of shame can account for much of what we know about shame and generate precise predictions. Here, we analyse the behavioural configuration that people adopt stereotypically when ashamed – slumped posture, downward head tilt, gaze avoidance, inhibition of speech – in light of shame's hypothesised function. This behavioural configuration may have differentially favoured its own replication by (a) hampering the transfer of information (e.g. diminishing audiences’ tendency to attend to or encode identifying information – shame camouflage) and/or (b) evoking less severe devaluative responses from audiences (shame display). The shame display hypothesis has received considerable attention and empirical support, whereas the shame camouflage hypothesis has to our knowledge not been advanced or tested. We elaborate on this hypothesis and suggest directions for future research on the shame pose.

View all citing articles on Scopus

^☆: Some of this research also carried at the Smithsonian Tropical Research Institute, APO, Miami 34002, U.S.A.

^☆☆: This work was supported by Reagents fellowships and an Earle C. Anthony fellowship from the University og California, Davis, and Scholarly Studies assistantships from the Smithsonian Tropical Research Institute.

¹: Current address: Museum of Vertebrate Zoology, 2593 Life Sciences Building, University of California, Berkeley, California 94720, U.S.A.

View full text

Microbes, herbivory and the evolution of social behavior☆,☆☆

Abstract

Comp. Biochem. Physiol

Comp. Biochem. Physiol

J. theor. Biol

Am. J. Clin. Nutr

A. Rev. Ecol. Syst

Nature

Discovery (Peabody Museum, Yale)

The Ecology of Arboreal Folivores

Science

Am. Zool

Science

Paleobiology

Quart. Rev. Biol

Anat. Rec

Mem. Am. Acad. Arts Sci

Body Size, Digestive Capacity and Feeding Strategies of Herbivores

Ecology

Equine Vet. J

Am. Zool

Sci. Am

J. Herpetol

Nature

A Cold Look at the Warm-blooded Dinosaurs

The Rumen and its Microbes