Bat behavioral immune responses in social contexts: current knowledge and future directions

Animals often mount complex immune responses to infections. Aside from cellular and molecular defense mechanisms, animals can alter their behavior in response to infection by avoiding, resisting, or tolerating negative effects of pathogens. These behaviors are often connected to cellular and molecular immune responses. For instance, sickness behaviors are a set of behavioral changes triggered by the host inflammatory response (e.g., cytokines) and could aid in resisting or tolerating infection, as well as affect transmission dynamics if sick animals socially withdraw or are being avoided by others. To fully understand the group and population level transmission dynamics and consequences of pathogen infections in bats, it is not only important to consider cellular and molecular defense mechanisms, but also behavioral mechanisms, and how both interact. Although there has been increasing interest in bat immune responses due to their ability to successfully cope with viral infections, few studies have explored behavioral anti-pathogen defense mechanisms. My main objective is to explore the interaction of cellular and molecular defense mechanisms, and behavioral alterations that results from infection in bats, and to outline current knowledge and future research avenues in this field

Social distancing in nature : insights from vampire bats

I am broadly interested in how animals change their social behaviors in response to infection and how these changes affect pathogen spread across groups or populations. Hence, my research integrates ideas from behavioral ecology, epidemiology, and immunology to better understand the ultimate and proximate consequences of social distancing. In my first chapter, I synthesize literature on pathogen-induced changes in sociality in non-human animals and in humans. These include active and passive changes in pathogen-exposed and unexposed group members, occurring both before and after individuals develop an active infection. Behavioral changes that reduce social interactions and thus pathogen spread include changes driven by infectious hosts, such as sickness behaviors and active self-isolation, as well as changes driven by healthy hosts, including active avoidance or exclusion of infectious individuals and proactive social distancing in the face of pathogenic threats. I review what is known about underlying mechanism and consider implications for evolution and epidemiology. I also highlight the value of studying social distancing behaviors in non-human animals to better understand how these behaviors alter traits relevant to human public health, including pathogen spread and virulence. The remaining three chapters present my experimental work on common vampire bats (Desmodus rotundus) in Panama. In my second chapter, I established a method to experimentally induce transient symptoms of sickness in vampire bats by using injections of lipopolysaccharide (LPS). LPS injections mimic a bacterial infection including physiological, as well as behavioral symptoms (commonly termed ‘sickness behaviors’) in vampire bats (Stockmaier et al., 2018). Importantly, vampire bats also expressed a form a social distancing by reducing their allogrooming efforts towards others in this study (Stockmaier et al., 2018). In my third chapter I explored how this social distancing behavior in vampire bats is affected by what type of behavior is observed (allogrooming versus food sharing), how sociality as a biological trait is defined (e.g. network degree versus mean edge strength), and the type of relationship between two interacting individuals (kin versus non-kin relationship). Immune-challenged bats experienced a greater reduction in grooming than food sharing which potentially bestows greater fitness benefits (Stockmaier et al., 2020a). I also found that sickness effects on social behaviors might vary with relationship type because the immune challenge had smaller effects on mother-offspring interactions (Stockmaier et al., 2020a). Finally, I found that sickness effects depend on how a social interaction is defined (e.g. number of grooming partners versus grooming duration). I found that sickness reduced the number of grooming partners but less so the overall duration of social encounters (Stockmaier et al., 2020a). This reduction in grooming partners could be driven by reduced movement but could be augmented by reduced social vocalizations. When isolated, vampire bats produce contact calls that attract highly associated group mates. In my fourth chapter I explore whether LPS injections affect contact calling behavior. I show that LPS-induced sickness behavior mainly reduces the number of contact calls produced by isolated vampire bats (Stockmaier et al., 2020b). This effect is relevant for pathogen transmission in social animals that rely on vocalizations to maintain physical contact.Ecology, Evolution and Behavio

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Datasets and R.code: "Sickness behaviors in vampire bats (Desmodus rotundus)"

Fileset contains datasets as well as R. code supporting "sickness behavior reduces allogrooming in vampire bats". R- code "dyadic_social_grooming_analysis" contains simple model of how sickness induced changes in allogrooming given to other individuals, could affect disease transmission.<div><br></div><div>Detailed description of individual datasets:</div><div><br></div><div>(1) "physiology_data" and R-code "physiology_analysis"</div><div><div>group = Group the individual was housed in (1-7)</div><div>experiment = Week, experiment 1 = week 1, experiment 2 = week 2</div><div>individual = injected individual</div><div>treatment = treatment (LPS or PBS)</div><div>bm.postmpre = bodymass post injection minus bodymass pre-injection (grams)</div><div>WBC.postmpre = white blood cell concentration (cells/ml) post-injection minus pre-injection</div><div>NL.postmpre = NL ratio post-injection minus NL ratio pre-injection</div></div><div><br></div><div>(2) "individual_behaviors_means" and R-code "individual_behavior_analysis"</div><div><div>focal.bat: focal bat of behavior scoring after injection</div><div>treatment: treatment (LPS or PBS)</div><div>activity: mean activity rate of 2 hours observation ((counts hour 1 / onscreen counts) + (counts hour 2 / onscreen counts)) / 2</div><div>sleep.rate: mean sleep rate of 2 hours observation ((counts hour 1 / onscreen counts) + (counts hour 2 / onscreen counts)) / 2</div><div>grooming.rate: mean self-grooming rate of 2 hours observation ((counts hour 1 / onscreen counts) + (counts hour 2 / onscreen counts)) / 2</div><div>ml.rate: mean mouthlicking rate of 2 hours observation ((counts hour 1 / onscreen counts) + (counts hour 2 / onscreen counts)) / 2</div><div>socgroom.rate: mean social grooming rate of 2 hours observation ((counts hour 1 / onscreen counts) + (counts hour 2 / onscreen counts)) / 2</div><div>moving.rate: mean moving rate of 2 hours observation ((counts hour 1 / onscreen counts) + (counts hour 2 / onscreen counts)) / 2</div><div>group: group the focal bat was housed in (from 1-7)</div><div>groupsize: groupsize of the group the focal bat was housed in (2 or 4)</div></div><div><br></div><div>(3) "dyadic_social_grooming_dataset" and R-code "dyadic.social.grooming.analysis"</div><div><div>focal.bat: focal bat of observation</div><div>partner: partner bat the focal bat was interacting with</div><div>pair: description of two interacting bats as a pair</div><div>group: group the focal bat was housed in (groups 1-7)</div><div>groupsize: groupsize of the group the focal bat was housed in (2 or 4)</div><div>day.in.exp: Day on the experimental timeline (see figure S1)</div><div>week: Week in the experiment (week 1 or 2)</div><div>duration.rec: duration in seconds the focal bat received grooming from partner</div><div>duration.act: duration in seconds the focal bat gave grooming to partner</div><div>hours.rec: hours recorded (always 2 h except for nights 5 and 13 due to technical problems)</div><div>dir.dyad: unique description of a pair of two bats. Directional dyad, e.g focal bat is A and partner is B so directional dyad is B->A</div><div>treatment: treatment during the experimental week 1 or 2</div><div>injection: injection = "no" for baseline nights and "yes" for nights when the focal bat was injected with either LPS or PBS</div></div

Behavioural defences against parasites across host social structures

Animals exhibit a variety of behavioural defences against socially transmitted parasites. These defences evolved to increase host fitness by avoiding, resisting or tolerating infection. Because they can occur in both infected individuals and their uninfected social partners, these defences often have important consequences for the social group. Here, we discuss the evolution and ecology of anti-parasite behavioural defences across a taxonomically wide social spectrum, considering colonial groups, stable groups, transitional groups and solitary animals. We discuss avoidance, resistance and tolerance behaviours across these social group structures, identifying how social complexity, group composition and interdependent social relationships may contribute to the expression and evolution of behavioural strategies. Finally, we outline avenues for further investigation such as approaches to quantify group-level responses, and the connection of the physiological and behavioural response to parasites in different social contexts

Infectious diseases and social distancing in nature

Final manuscript draft for review article "Infectious diseases and social distancing in nature" (Science 05 Mar 2021; link to published article: https://science.sciencemag.org/content/371/6533/eabc8881