Expanded diversity of novel hemoplasmas in rare and undersampled Neotropical bats.

Hemotropic mycoplasmas are emerging as a model system for studying bacterial pathogens in bats, but taxonomic coverage of sampled host species remains biased. We leveraged a long-term field study in Belize to uncover novel hemoplasma diversity in bats by analyzing 80 samples from 19 species, most of which are infrequently encountered. PCR targeting the partial 16S rRNA gene found 41% of bats positive for hemoplasmas. Phylogenetic analyses found two novel host shifts of hemoplasmas, four entirely new hemoplasma genotypes, and the first hemoplasma detections in four bat species. One of these novel hemoplasmas (from Neoeptesicus furinalis) shared 97.6% identity in the partial 16S rRNA gene to a human hemoplasma (Candidatus Mycoplasma haemohominis). Additional analysis of the partial 23S rRNA gene allowed us to also designate two novel hemoplasma species, in Myotis elegans and Phyllostomus discolor, with the proposed names Candidatus Mycoplasma haematomyotis sp. nov. and Candidatus Mycoplasma haematophyllostomi sp. nov., respectively. Our analyses show that additional hemoplasma diversity in bats can be uncovered by targeting rare or undersampled host species.

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 effects of rabies infection in male vampire bats (Desmodus rotundus).

Rabies virus (RABV) transmitted by the common vampire bat (Desmodus rotundus) poses a threat to agricultural development and public health throughout the Neotropics. The ecology and evolution of rabies host-pathogen dynamics are influenced by two infection-induced behavioural changes. RABV-infected hosts often exhibit increased aggression which facilitates transmission, and rabies also leads to reduced activity and paralysis prior to death. Although several studies document rabies-induced behavioural changes in rodents and other dead-end hosts, surprisingly few studies have measured these changes in vampire bats, the key natural reservoir throughout Latin America. Taking advantage of an experiment designed to test an oral rabies vaccine in captive male vampire bats, we quantify for the first time, to our knowledge, how rabies affects allogrooming and aggressive behaviours in this species. Compared to non-rabid vampire bats, rabid individuals reduced their allogrooming prior to death, but we did not detect increases in aggression among bats. To put our results in context, we review what is known and what remains unclear about behavioural changes of rabid vampire bats (resumen en español, electronic supplementary material, S1).

Infectious diseases and social distancing in nature.

Spread of contagious pathogens critically depends on the number and types of contacts between infectious and susceptible hosts. Changes in social behavior by susceptible, exposed, or sick individuals thus have far-reaching downstream consequences for infectious disease spread. Although "social distancing" is now an all too familiar strategy for managing COVID-19, nonhuman animals also exhibit pathogen-induced changes in social interactions. Here, we synthesize the effects of infectious pathogens on social interactions in animals (including humans), review what is known about underlying mechanisms, and consider implications for evolution and epidemiology.

Immune-challenged vampire bats produce fewer contact calls.

Vocalizations are an important means to facilitate social interactions, but vocal communication may be affected by infections. While such effects have been shown for mate-attraction calls, other vocalizations that facilitate social contact have received less attention. When isolated, vampire bats produce contact calls that attract highly associated groupmates. Here, we test the effect of an immune challenge on contact calling rates of individually isolated vampire bats. Sickness behaviour did not appear to change call structure, but it decreased the number of contact calls produced. This effect could decrease contact with groupmates and augment other established mechanisms by which sickness reduces social encounters (e.g. mortality, lethargy and social withdrawal or disinterest).

Sickness effects on social interactions depend on the type of behaviour and relationship.

Infections can change social behaviour in multiple ways, with profound impacts on pathogen transmission. However, these impacts might depend on the type of behaviour, how sociality as a biological trait is defined (e.g. network degree vs. mean edge strength) and the type of social relationship between the interacting individuals. We used the highly social common vampire bat Desmodus rotundus to test how an immune challenge by lipopolysaccharide (LPS) injections affects two different social behaviours and three alternate measures of sociality, and whether the LPS effect differs by kinship relationship. Effects of sickness should be lower for social behaviours that bestow greater benefits to inclusive fitness, such as food sharing. As predicted, immune-challenged bats experienced a greater reduction in allogrooming received than food sharing received. Sickness effects might also depend on how a social interaction is defined (e.g. the number of grooming partners vs. the duration of grooming events). We predicted that sickness would impact both the number and duration of social encounters, but we only detected a decrease in the number of grooming partners. Finally, sickness effects might vary with social relationship type. We predicted that sickness effects should be smaller for interactions among close kin. As expected, the immune challenge had smaller effects on mother-offspring interactions. In conclusion, our results highlight the need to explicitly consider how the effects of sickness on social network structure can differ depending on the 'who, what, and how' of social interactions, because these factors are likely to influence how sickness behaviour alters pathogen transmission.

No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat.

Bat immune systems may allow them to respond to zoonotic agents more efficiently than other mammals. As the first line of defence, the taxonomically conserved acute phase immune reaction of leucocytosis and fever is crucial for coping with infections, but it is unknown if this response is a key constituent to bat immunological success. We investigated the acute phase reaction to a standard lipopolysaccharide (LPS) challenge in Pallas's mastiff bats (Molossus molossus). Challenged bats lost mass, but in contrast to other mammals showed no leucocytosis or fever. There also was no influence on body temperature reduction during torpor. When compared to recent genome-wide assays for constituent immune genes, this lack of a conserved fever response to LPS contributes to a clearer understanding of the innate immune system in bat species and of the coevolution of bats with a wide diversity of pathogens.