Genetic diversity, infection prevalence, and possible transmission routes of Bartonella spp. in vampire bats

Bartonella spp. are globally distributed bacteria that cause endocarditis in humans and domestic animals. Recent work has suggested bats as zoonotic reservoirs of some human Bartonella infections; however, the ecological and spatiotemporal patterns of infection in bats remain largely unknown. Here we studied the genetic diversity, prevalence of infection across seasons and years, individual risk factors, and possible transmission routes of Bartonella in populations of common vampire bats (Desmodus rotundus) in Peru and Belize, for which high infection prevalence has previously been reported. Phylogenetic analysis of the gltA gene for a subset of PCR-positive blood samples revealed sequences that were related to Bartonella described from vampire bats from Mexico, other Neotropical bat species, and streblid bat flies. Sequences associated with vampire bats clustered significantly by country but commonly spanned Central and South America, implying limited spatial structure. Stable and nonzero Bartonella prevalence between years supported endemic transmission in all sites. The odds of Bartonella infection for individual bats was unrelated to the intensity of bat flies ectoparasitism, but nearly all infected bats were infested, which precluded conclusive assessment of support for vector-borne transmission. While metagenomic sequencing found no strong evidence of Bartonella DNA in pooled bat saliva and fecal samples, we detected PCR positivity in individual saliva and feces, suggesting the potential for bacterial transmission through both direct contact (i.e., biting) and environmental (i.e., fecal) exposures. Further investigating the relative contributions of direct contact, environmental, and vector-borne transmission for bat Bartonella is an important next step to predict infection dynamics within bats and the risks of human and livestock exposures

Predictors and immunological correlates of sublethal mercury exposure in vampire bats

Mercury (Hg) is a pervasive heavy metal that often enters the environment from anthropogenic sources such as gold mining and agriculture. Chronic exposure to Hg can impair immune function, reducing the ability of animals to resist or recover from infections. How Hg influences immunity and susceptibility remains unknown for bats, which appear immunologically distinct from other mammals and are reservoir hosts of many pathogens of importance to human and animal health. We here quantify total Hg (THg) in hair collected from common vampire bats (Desmodus rotundus), which feed on blood and are the main reservoir hosts of rabies virus in Latin America. We examine how diet, sampling site and year, and bat demography influence THg and test the consequences of this variation for eight immune measures. In two populations from Belize, THg concentrations in bats were best explained by an interaction between long-term diet inferred from stable isotopes and year. Bats that foraged more consistently on domestic animals exhibited higher THg. However, relationships between diet and THg were evident only in 2015 but not in 2014, which could reflect recent environmental perturbations associated with agriculture. THg concentrations were low relative to values previously observed in other bat species but still correlated with bat immunity. Bats with higher THg had more neutrophils, weaker bacterial killing ability and impaired innate immunity. These patterns suggest that temporal variation in Hg exposure may impair bat innate immunity and increase susceptibility to pathogens such as bacteria. Unexpected associations between low-level Hg exposure and immune function underscore the need to better understand the environmental sources of Hg exposure in bats and the consequences for bat immunity and susceptibility

Livestock abundance predicts vampire bat demography, immune profiles, and bacterial infection risk

Human activities create novel food resources that can alter wildlife–pathogen interactions. If resources amplify or dampen, pathogen transmission probably depends on both host ecology and pathogen biology, but studies that measure responses to provisioning across both scales are rare. We tested these relationships with a 4-year study of 369 common vampire bats across 10 sites in Peru and Belize that differ in the abundance of livestock, an important anthropogenic food source. We quantified innate and adaptive immunity from bats and assessed infection with two common bacteria. We predicted that abundant livestock could reduce starvation and foraging effort, allowing for greater investments in immunity. Bats from high-livestock sites had higher microbicidal activity and proportions of neutrophils but lower immunoglobulin G and proportions of lymphocytes, suggesting more investment in innate relative to adaptive immunity and either greater chronic stress or pathogen exposure. This relationship was most pronounced in reproductive bats, which were also more common in high-livestock sites, suggesting feedbacks between demographic correlates of provisioning and immunity. Infection with both Bartonella and haemoplasmas were correlated with similar immune profiles, and both pathogens tended to be less prevalent in high-livestock sites, although effects were weaker for haemoplasmas. These differing responses to provisioning might therefore reflect distinct transmission processes. Predicting how provisioning alters host–pathogen interactions requires considering how both within-host processes and transmission modes respond to resource shifts

Data from: An experimental test of the relationship between yolk testosterone and the social environment in a colonial passerine

Maternal hormones can be transferred to offspring during prenatal development in response to the maternal social environment, and may adaptively alter offspring phenotype. For example, numerous avian studies show that aggressive competition with conspecifics tends to result in females allocating more testosterone to their egg yolks, and this may cause offspring to have more competitive phenotypes. However, deviations from this pattern of maternal testosterone allocation are found, largely in studies of colonial species, and have yet to be explained. Colonial species may have different life-history constraints causing different yolk testosterone allocation strategies in response to conspecific competition, but few studies have experimentally tested whether colonial species do indeed differ from that of solitary species. To test this, we collected eggs from zebra finches (Taeniopygia guttata), a colonial species, in the presence and absence of conspecific intrusions. Females did not alter the concentration of testosterone deposited in eggs laid during intrusions despite becoming more aggressive. These results suggest that maternal effects are not characterized by a uniform response to the social environment, but rather need to be contextualized with life-history traits

Electronic supplementary material: Details of species included in the meta-analysis (Table S1), flow diagram of the inclusion process for published articles in the analysis (Fig. S1), a funnel plot testing for publishing bias (Fig. S2), and all associated references. from Evolutionary implications of interspecific variation in a maternal effect: a meta-analysis of yolk testosterone response to competition

Competition between conspecifics during the breeding season can result in behavioural and physiological programming of offspring via maternal effects. For birds, in which maternal effects are best studied, it has been claimed that exposure to increased competition causes greater deposition of testosterone into egg yolks, which creates faster growing, more aggressive offspring; such traits are thought to be beneficial for high-competition environments. Nevertheless, not all species show a positive relationship between competitive interactions and yolk testosterone, and an explanation for this interspecific variation is lacking. We here test if the magnitude and direction of maternal testosterone allocated to eggs in response to competition can be explained by life-history traits while accounting for phylogenetic relationships. We performed a meta-analysis relating effect size of yolk testosterone response to competition with species coloniality, nest type, parental effort and mating type. We found that effect size was moderated by coloniality and nest type; colonial species and those with open nests allocate less testosterone to eggs when in more competitive environments. Applying a life-history perspective helps contextualize studies showing little or negative responses of yolk testosterone to competition and improves our understanding of how variation in this maternal effect may have evolved

Data from: Relationship between maternal environment and DNA methylation patterns of estrogen receptor alpha in wild Eastern Bluebird (Sialia sialis) nestlings: a pilot study

There is mounting evidence that, across taxa, females breeding in competitive environments tend to allocate more testosterone to their offspring prenatally and these offspring typically have more aggressive and faster-growing phenotypes. To date, no study has determined the mechanisms mediating this maternal effect's influence on offspring phenotype. However, levels of estrogen receptor alpha (ERα) gene expression are linked to differences in early growth and aggression; thus, maternal hormones may alter gene regulation, perhaps via DNA methylation, of ERα in offspring during prenatal development. We performed a pilot study to examine natural variation in testosterone allocation to offspring through egg yolks in wild Eastern Bluebirds (Sialia sialis) in varying breeding densities and percent DNA methylation of CG dinucleotides in the ERα promoter in offspring brain regions associated with growth and behavior. We hypothesized that breeding density would be positively correlated with yolk testosterone, and prenatal exposure to maternal-derived yolk testosterone would be associated with greater offspring growth and decreased ERα promoter methylation. Yolk testosterone concentration was positively correlated with breeding density, nestling growth rate, and percent DNA methylation of one out of five investigated CpG sites (site 3) in the diencephalon ERα promoter, but none in the telencephalon (n = 10). Percent DNA methylation of diencephalon CpG site 3 was positively correlated with growth rate. These data suggest a possible role for epigenetics in mediating the effects of the maternal environment on offspring phenotype. Experimentally examining this mechanism with a larger sample size in future studies may help elucidate a prominent way in which animals respond to their environment. Further, by determining the mechanisms that mediate maternal effects, we can begin to understand the potential for the heritability of these mechanisms and the impact that maternal effects are capable of producing at an evolutionary scale

Data from: Genetic diversity, infection prevalence, and possible transmission routes of Bartonella spp. in vampire bats

Bartonella spp. are globally distributed bacteria that cause endocarditis in humans and domestic animals. Recent work has suggested bats as zoonotic reservoirs of some human Bartonella infections; however, the ecological and spatiotemporal patterns of infection in bats remain largely unknown. Here we studied the genetic diversity, prevalence of infection across seasons and years, individual risk factors, and possible transmission routes of Bartonella in populations of common vampire bats (Desmodus rotundus) in Peru and Belize, for which high infection prevalence has previously been reported. Phylogenetic analysis of the gltA gene for a subset of PCR-positive blood samples revealed sequences that were related to Bartonella described from vampire bats from Mexico, other Neotropical bat species, and streblid bat flies. Sequences associated with vampire bats clustered significantly by country but commonly spanned Central and South America, implying limited spatial structure. Stable and nonzero Bartonella prevalence between years supported endemic transmission in all sites. The odds of Bartonella infection for individual bats was unrelated to the intensity of bat flies ectoparasitism, but nearly all infected bats were infested, which precluded conclusive assessment of support for vector-borne transmission. While metagenomic sequencing found no strong evidence of Bartonella DNA in pooled bat saliva and fecal samples, we detected PCR positivity in individual saliva and feces, suggesting the potential for bacterial transmission through both direct contact (i.e., biting) and environmental (i.e., fecal) exposures. Further investigating the relative contributions of direct contact, environmental, and vector-borne transmission for bat Bartonella is an important next step to predict infection dynamics within bats and the risks of human and livestock exposures

Becker et al PLoS NTD_data

Individual-level data on Bartonella infection status as determined by PCR targeting gltA and relevant vampire bat covariates

Corticosterone and testosterone treatment influence expression of gene pathways linked to meiotic segregation in preovulatory follicles of the domestic hen.

Decades of work indicate that female birds can control their offspring sex ratios in response to environmental and social cues. In laying hens, hormones administered immediately prior to sex chromosome segregation can exert sex ratio skews, indicating that these hormones may act directly on the germinal disc to influence which sex chromosome is retained in the oocyte and which is discarded into an unfertilizable polar body. We aimed to uncover the gene pathways involved in this process by testing whether treatments with testosterone or corticosterone that were previously shown to influence sex ratios elicit changes in the expression of genes and/or gene pathways involved in the process of meiotic segregation. We injected laying hens with testosterone, corticosterone, or control oil 5h prior to ovulation and collected germinal discs from the F1 preovulatory follicle in each hen 1.5h after injection. We used RNA-sequencing (RNA-seq) followed by DESeq2 and gene set enrichment analyses to identify genes and gene pathways that were differentially expressed between germinal discs of control and hormone-treated hens. Corticosterone treatment triggered downregulation of 13 individual genes, as well as enrichment of gene sets related to meiotic spindle organization and chromosome segregation, and additional gene sets that function in ion transport. Testosterone treatment triggered upregulation of one gene, and enrichment of one gene set that functions in nuclear chromosome segregation. This work indicates that corticosterone can be a potent regulator of meiotic processes and provides potential gene targets on which corticosterone and/or testosterone may act to influence offspring sex ratios in birds

Maternal environment and DNA methylation patterns

Data collected in the field for 26 Eastern bluebird nests and the one randomly selected nestling from each of the 25 successfully hatched nests. Nest data include yolk testosterone, breeding density, clutch size, and brood size. Nestling data include sex, mass, growth rate, and methylation patterns