Microbes and Animal Behavior

Bella Microbio 238 2020

Introduction

By [Bella Stevens]
Animal behavior can be influenced by many factors, making it an interesting yet complex field. From environmental interactions to genetics, there are many ways to look at a certain behavior. How do microbes, particularly bacteria, play a role? Can these microscopic organisms that live inside animals affect who these animals mate with or even how they communicate with conspecifics? Experiments have used genetics, such as rRNA analysis, to study the make-up of symbiotic microbial communities to further understand a certain behavior, like finding another piece to the puzzle. Because animal behavior covers a wide range of topics, from mating to communication, there are possibly many ways microbes, especially symbiotic microbes, could affect behavior in a variety of animals from hyenas to squids, and even humans. How microbes affect and interact with animals can give us insight into our own relationship with microbial organisms and help us understand our own behavior.

Section 1

Microbe-animal interactions are often seen in the form of symbiosis, and these relationships impact various animal behaviors from mate choice to interspecies communication. These reactions range widely from parasitic to mutualistic. Marine animals in particular act as hosts for a diverse range of symbiotic microbes, with at least 7 different phyla acting as hosts for chemosynthetic symbionts. In terms of behavior and physiology, there is a diversity of reductants and oxidants that hosts provide for their symbionts. For example, motile animals such as nematode worms migrate between upper oxidized and lower reduced sediment layers to obtain oxidants and reductants. Thyasirid clams even use their feet, which extend up to 30 times the length of their shells,to form burrows, with the length and number of burrows corresponding to the concentration of hydrogen sulfide in the sediment (1).

There are also many examples in the animal kingdom of gut microbiota influencing animal behavior. For instance, research has shown that commensal bacteria can affect mating in flies (2). After one generation, flies preferred to mate with those that were on the same diet, either starch or molasses, and these preferences continued for at least 37 generations. This 2010 study hypothesized that the change in diet, i.e. rearing the first group of flies on either starch or molasses, altered their gut microbiome and influenced their behavior. Aside from the clear correlation between diet and mating choice, this was further confirmed by antibiotic treatment which caused the mating choices to become totally random, indicating that microbiota played a role in the previously seen preferences. Additionally, analysis of fly rRNA found that flies transferred to starch contained a much higher percentage of Lactobacillus plantarum than the flies raised on standard cornmeal-molasses-yeast (CMY), which the paper suggests influences behavior via the influencing the level of sex pheromones. Gut microbiota not only affects behavior in insects but in vertebrate animals such as mammals. A 2010 study looked at gut microbiota in mice and the effect on behavior and even brain development. Previous studies had found that exposure to some microbial pathogens in certain developmental periods resulted in behavioral abnormalities. A 2010 study hypothesized that a normal gut microbiota plays an important role in the environmental factors that modulate brain development and function (3).

Another instance of microbes playing an important role in animal development is seen in marine animals like the squid. Microbial symbionts can either be vertically or horizontally transmitted. Developmental programs must be altered to accommodate the symbiotic relationship, and establish the correct partners and not interlopers. A 2014 review examined what is known about the symbiotic relationship between the bacteria, Vibrio fischeri, and the Hawaiian bobtail squid, Euprymna scolopes (4). Juvenile squids are colonized in the light organ soon after hatching, the symbiont being obligate for the hosts but not dependent on the host themselves. Within hours of hatching, the juvenile squid has a colonized, bioluminescent organ. This symbiotic relationship is initiated by ventilating the surrounding seawater through the squid’s body cavity, harvesting V. fischeri while excluding other bacterial species. The cells aggregate along the ciliated epithelia, then move into the deep tissues. Finally, a few inoculating V. fischeri cells will fill crypts in the light organ. Vibrio fischeri are bioluminescent bacteria that produce light used by squid hosts as camouflage, an antipredator behavior also known as “counterillumination” that mimics moonlight and starlight. Researchers are also looking into the genome of Vibrio fischeri to better understand how these respiring bacteria generate energy, and what possible role they play in the global carbon cycle (5).

Section 2

Microbes can be involved in animal communication, with the animal host utilizing microbial products as signals that communicate social rank or group membership. Also note that a signal is not the same thing as a cue. A signal is an evolved act or structure that can either benefit the signaler or receiver, or both. A cue is a feature of the environment that may be beneficial but it doesn’t evolve. There are many modes of signaling, such as chemical signals like pheromones. In order to determine if a signal is mediated by microbes, scientists must demonstrate that the chemical signal can be synthesized by the microbiota, and if elimination of the microbiota results in a loss of the behavioral trait (6). Chemical communication comes in many forms. Some animals can synthesize their own chemical signals, while others rely on their environment or symbiotic microbes to obtain the components required for the signal.

Theis et al. (2012) studied microbial-mediated chemical communication in hyenas, specifically fermentative bacteria found in the hosts’ specialized mammalian scent glands (7). The study’s findings coincide with the fermentation hypothesis for chemical recognition which states that fermentative bacteria in scent glands generate odorants used by the hosts in communication and that variation in odors is due to the variation in the bacterial communities of the scent glands. A phylogenetic analysis was conducted, and showed that the hyena scent pouch microbiota was made up of mostly obligate or facultative anaerobes closely related to well-documented odor producers. Theis et al. (2012) also found group-specific bacterial communities from the hyenas’ scent pouches. One possible mechanism for this is that Spotted hyenas frequently scent mark where other members have marked as well, thus creating a possible pathway for transmission of bacterial communities among members within a clan.

Another study found that male bats (Saccopteryx bilineata) have a pouch-like scent organ in the leading wing membrane that contains an odorous liquid involved in courtship (8). Voig et al. (2005) studied the microbial flora within these scent organs to determine if microbial degradation of scents influences a male’s mating success by affecting his scent. During courtship, female preference is important so males must attempt to court females by hovering over them, and fanning their scents towards the females. Everyday males transfer genital and glular liquids into the wing sacs. This 2005 study predicts that males repeat this process in order to minimize microbial fermentation and control the microflora in their wing sacs, which create a scent specific to the individual. This prediction was supported by their findings that microbial diversity was lower in males than females, and that individual males on average carried two microbial strands in their wing sacs.

Many mammal species are able to distinguish between different individuals by their odor. The African dwarf mongoose, Helogale undulata, uses odors produced by anal glands to communicate. Additionally, these mammals can distinguish the marks made by the anal glands of conspecifics. Specifically, the “anal pockets” of an individual has a unique concentration of various carboxylic acid products from bacterial breakdown of sedum and apocrine secretion. Gorman (1976) found that mongooses can discriminate between the anal pocket contents of other mongooses and even synthetic odors (9).

Section 3

Understanding the ways in which microbes affect animal behavior can help us understand certain disorders in people. The gut microbiota in mammals is essential for digestion, immunity and normal host physiology. One additional and unexpected role is in brain function via the “microbiota-gut-brain axis”.

Previous research has found that animals raised without microbial colonization show abnormal behavior. And now, recent studies have seen a possible link between gut microbiota and Autism Spectrum Disorder (ASD). For instance, Vuong and Hsiao (2017) reviewed studies of microbial dysbiosis (an impaired microbiota) in ASD (10). Features of ASD in humans include social communication deficiencies, repetitive behaviors/motor movements and other behavioral abnormalities (anxiety, seizures, hyperactivity). Studies that used mice models to examine social behavior in germ-free mice found that germ-free mice were less sociable, interacting with nonsocial objects instead of other mice or preferring to only interact with familiar mice rather than unfamiliar (11,12). Additionally, other researchers have found that these behavioral abnormalities could be corrected in germ-free mice by postnatal colonization with a wild-type gut microbiota at weaning (13). It has recently been found that the maternal diet is a perinatal risk factor, at least in mice studies. Buffington et al. (2016) found that maternal obesity induced by a high-fat diet in mice alters the gut microbiome in offspring, resulting in social behavioral deficits which were corrected with transfer of a gut microbiome from control mice (14). Moreover, treatment with the gut bacteria Lactobacillus reuteri alone sufficiently restored social behaviors. The success of the gut microbiome was connected with its ability to promote hypothalamic levels of oxytocin, a hormone released in social bonding, also known as the “love hormone”, and neuron activation in the ventral tegmental area, a brain region which has many functions including emotion output from the amygdala.

References

Authored for BIOL 238 Microbiology, taught by Joan Slonczewski, 2018, Kenyon College.