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Biology subjects

Martin, L. B.

Publications and source records attributed to Martin, L. B..

11 recordsLinked to original sources

Climate drives geographic variation in individual Peromyscus leucopus immunity against zoonotic disease.

Geographic variation in host immunity could have major influences on disease dynamics, including zoonotic forms that affect humans. Such variation in immunity could be driven by variation in climate, either directly or, more likely, indirectly via resource availability. We compared the immune gene expression of wild Peromyscus leucopus mice, the primary reservoir for the bacterium that causes Lyme disease, Borrelia burgdorferi, among eight sites spanning 1,400 km of the northeastern United States. We discovered that climate conditions at sites strongly predicted immunity to the most common zoonotic pathogen in the U.S.: mice from warmer, wetter sites were more prepared to resist B. burgdorferi infections. Our results reveal a novel pathway by which climate change could affect pathogen spillover or zoonotic epidemics generally.

immunology↗

Movement-related drivers of exposure to West Nile virus by American robins (Turdus migratorius)

The ecological processes that determine how individual animals become hosts to zoonotic pathogens is a topic of rapidly growing interest. However, how such exposure is mediated by context (e.g., season, location), host behavior (e.g., migration distance) and host demographics is generally poorly understood. We evaluated seasonal exposure to West Nile Virus of American robins sampled in Indiana and compared our results to those of previous studies. Because robins that breed in Indiana are partial migrants (i.e., only a portion of the population migrates), we evaluated their probability of exposure to WNV as a function of whether they migrated or not and of their movement distance. We also tagged a subset of breeding robins with tracking devices to evaluate their potential to disperse the virus between Indiana and other regions of the continent. We found that robins that breed in Indiana are exposed to WNV at a higher rate than that detected in previous studies, but found no correlation between robin exposure and whether a robin migrated or not, nor with migration distance, season, sex, and breeding latitude (for robins overwintering in Indiana). Our tracking data indicate that robins that breed in Indiana migrate several hundred miles to overwinter in the southeastern US. The mean duration of their return to Indiana in spring is 10.3 days, which is less than the maximum infectious period found for robins in previous studies, suggesting that they have the capacity to move WNV long distances in spring. However, we still know little about the physiological capacity of robins to migrate while being infectious, which could inhibit the dispersal of the virus through robin migration. Future research on the physiological, ecological and behavioral factors mediating the exposure of birds to WNV will lend insight into the role that robins and other birds play in the transmission ecology of the virus.

ecology↗

Bacterial sepsis triggers stronger transcriptomic responses in larger primates

Empirical data relating body mass to immune defense against infections remain limited. Although the Metabolic Theory of Ecology predicts that larger organisms would have weaker immune responses, recent studies have suggested that the opposite may be true. These discoveries have led to the Safety Factor hypothesis, which proposes that larger organisms have evolved stronger immune defenses because they carry greater risks of exposure to pathogens and parasites. In this study, we simulated sepsis by exposing blood from nine primate species to a bacterial lipopolysaccharide (LPS), measured the relative expression of immune and other genes using RNAseq, and fit phylogenetic models to determine how gene expression was related to body mass. In contrast to non-immune-annotated genes, we discovered hypermetric scaling in the LPS-induced expression of innate immune genes, such that large primates had a disproportionately greater increase in gene expression of immune genes compared to small primates. Hypermetric immune gene expression appears to support the Safety Factor hypothesis, though this pattern may represent a balanced evolutionary mechanism to compensate for lower per-transcript immunological effectiveness. This study contributes to the growing body of immune allometry research, highlighting its importance in understanding the complex interplay between body size and immunity over evolutionary timescales. Author SummaryUnderstanding the relationship between an animals size and its ability to defend against disease can inform predictions about evolutionary tradeoffs and susceptibility to infection. Two major theories - the Metabolic Theory of Ecology (MTE) and the Safety Factor hypothesis - offer opposing views on how body size influences it immune defenses. In this study, we compared the immune gene expression of nine primate species to a simulated bacterial infection. We found that larger species mounted a stronger transcriptional immune response, consistent with either the Safety Factor hypothesis or an evolutionary pressure to compensate for and balance the effects expected in the context of the MTE.

evolutionary biology↗

Host stress hormones affect host, but not vector, infectiousness for West Nile virus

Hormones that help hosts cope with stressors also affect how hosts regulate the processes that influence their susceptibility to parasites as well as their propensity to transmit pathogens to other hosts and vectors. In birds, corticosterone (CORT), influences timing of activity, feeding behaviors, and various immune defenses that influence the number and outcomes of host interactions with vectors and parasites. No study to our knowledge, though, has investigated whether CORT in hosts affects the extrinsic incubation period (EIP) of a vector for a virus, one of the strongest drivers of vector-borne disease cycles. Our goal here was to discern whether experimental CORT alterations in zebra finches (Taeniopygia guttata) affected EIP for West Nile virus (WNV) in the mosquito, Culex quinquefasciatus, a common vector of WNV and other infections in the southern US. We experimentally manipulated CORT in birds, infected them with WNV, and then investigated whether EIP differed between vectors fed on CORT-treated or control birds. Although CORT enhanced WNV viremia in hosts, as we have observed previously, we found no effects of CORT on vector EIP or post-feeding mortality rates, another important component of epidemiological models. These results, plus our prior observations that CORT enhances host attractiveness, indicate that some but not all stages of host-vector-virus interactions are sensitive to host stress.

ecology↗

FKBP5 expression is related to HPA flexibility and the capacity to cope with stressors in the house sparrow

The hypothalamic-pituitary-adrenal (HPA) axis and its end products, the glucocorticoids, are critical to responding appropriately to stressors. Subsequently, many studies have sought relationships between glucocorticoids and measures of health or fitness, but such relationships are at best highly context dependent. Recently, some endocrinologists have started to suggest that a focus on HPA flexibility, the ability of an individual to mount appropriate responses to different stressors, could be useful. Here, we tested the hypothesis that expression of FKBP5, a cochaperone in the glucocorticoid receptor complex, is a simple and reliable proxy of HPA flexibility in a wild songbird, the house sparrow (Passer domesticus). We quantified HPA flexibility in a novel way, using guidance from research on heart rhythm regulation. As predicted, we found that adult sparrows with low stress-induced FKBP5 expression in the hypothalamus exhibited high HPA flexibility. Moreover, low FKBP5 expression was associated with better stress coping capacities in terms of exploratory disposition and body mass maintenance. Altogether, these results suggest that FKBP5 may be important in the regulation HPA flexibility, potentially affecting how individuals cope with natural and anthropogenic adversity.

physiology↗

Body size affects immune cell proportions in birds and non-volant mammals, but not bats

Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints likely have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a scaling framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells--lymphocytes, and granulocytes (neutr-/heterophils)--across 60 bat species, 414 bird species, and 256 non-volant mammal species. By using phylogenetically-informed statistical models on field-collected data from wild Neotropical bats, data gleaned from other wild bats available in the literature, and data from captive non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Future comparative studies of wild bats, birds, and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense. Summary statementPowered flight might constrain morphology such that certain immunological features are prioritized. We show that bats largely have similar cell proportions across body mass compared to strong allometric scaling relationships in birds and non-flying mammals.

physiology↗

Extreme hyperallometry of mammalian antibacterial defenses

Terrestrial mammals span 7 orders of magnitude in body size, ranging from the < 2 g pygmy shrew (Suncus etruscus) to the > 3900 kg African elephant (Loxodonta africana). Although body size has profound effects on the behavior, physiology, ecology, and evolution of animals, how investment in immune defenses changes with body size is unknown. Here, we develop a novel 12-point dilution-curve approach to describe and compare antibacterial capacity against 3 bacterial species among >160 terrestrial species of mammals. We show that antibacterial activity in serum across mammals exhibits isometry, but the serum of large mammals is less hospitable to bacteria than would be predicted by their metabolic rates. Specifically, hypometric metabolic rates would predict that a large species should have disproportionately lower antibacterial capacity than small species, but body size is unrelated to killing capacity across species. Scaling of antibacterial immune defenses provides novel perspectives on the ecology of host-pathogen interactions, and on their co-evolutionary dynamics. These results have direct implications for effectively modeling the evolution of immune defenses and identifying potential reservoir hosts of zoonotic pathogens.

ecology↗

Light pollution affects West Nile virus exposure risk across Florida.

Emerging infectious diseases (EIDs), including zoonotic arboviruses, present a global health threat. Multiple components of human land use change have been linked to arboviral emergence, but one pervasive factor that has received comparatively little attention is light pollution. Although often considered a component of built environments, artificial light at night (ALAN) outpaces the growth and spatial extent of urbanization, and thus affects areas where human population density and anthropogenic land changes are modest. West Nile virus (WNV) emergence has been described as peri-urban, but recent research suggests that its relative ubiquity in human-altered environments might actually be due to ALAN. Indeed, we found previously that experimental ALAN exposure enhanced avian competence to transmit WNV to mosquitoes. In the present study, we asked whether such organismal effects manifest ecologically by determining whether WNV exposure among sentinel chickens in Florida is related to local ALAN conditions. We found strong support for a nonlinear relationship between ALAN and WNV exposure in chickens with peak WNV risk occurring at low ALAN levels. Importantly, effects of ALAN on WNV exposure were stronger than other aspects of urbanization; only ambient temperature in the month prior to sampling had a comparable effect to ALAN. These results represent the first field evidence that ALAN might affect infectious disease exposure risk. We advocate for further research on how ALAN influences zoonotic risk, as well as efforts to study alternative nighttime lighting methods to reduce such risk. Significance StatementLight pollution associated with human development is a globally pervasive and rapidly expanding anthropogenic stressor; but despite documented effects on host immune functions and vector behaviors, how it affects infectious disease risk is unknown. Using data from the Florida Department of Health arbovirus surveillance program, we show that light pollution is a stronger predictor of variation in West Nile virus (WNV) exposure risk than many other previously implicated anthropogenic and natural environmental variables. Light pollution effects are nonlinear, so risk is highest in areas with dim light pollution. Our results highlight a new way that light pollution might affect human and wildlife health.

ecology↗

The impacts of body mass on immune cell concentrations in birds

Body mass affects many biological traits, but its impacts on immune defenses are fairly unknown. Recent research on mammals found that neutrophil concentrations scaled hypermetrically with body mass, a result not predicted by any existing theory. Although this mammalian model might predict how leukocyte concentrations scale with body mass in other vertebrates, vertebrate classes are distinct in many ways that might affect their current and historic interactions with parasites and hence the evolution of their immune systems. Subsequently, here, we asked which existing scaling hypothesis best-predicted relationships between body mass and lymphocyte, eosinophil, and heterophil concentrations--the avian functional equivalent of neutrophils--among >100 species of birds. We then examined the predictive power of body mass relative to life-history variation, as an extensive literature indicates that the scheduling of key life events has influenced immune system variation among species. Finally, we ask whether these scaling patterns differ from the patterns we observed in mammals. We found that an intercept-only model best-explained lymphocyte and eosinophil concentrations among birds; body mass minimally influenced these two cell types. For heterophils, however, body mass explained over 30% of the variation in concentrations among species, much more than life-history variation (~8%). As with mammalian neutrophils, avian heterophils scaled hypermetrically (b=0.19 {+/-} 0.05), but significantly steeper than mammals (~1.5x). As such, we discuss why birds might require more broadly-protective cells compared to mammals of the same body size. Body mass appears to have strong influences on the architecture of immune systems, which could impact host-parasite coevolution and even zoonotic disease risk for humans.

ecology↗

Epigenetic Potential and DNA Methylation in an Ongoing House Sparrow (Passer domesticus) Range Expansion

During range expansions, epigenetic mechanisms may mediate phenotypic responses to environmental cues, enabling organisms to adjust to novel conditions at novel sites. Here, we predicted that the number of CpG sites within the genome, one form of epigenetic potential, would be important for success during range expansions because DNA methylation can modulate gene expression and hence facilitate adaptive plasticity. Previously, we found that this same form of epigenetic potential was higher in introduced compared to native populations of house sparrows (Passer domesticus) for two immune genes (Toll-like receptors 2A and 4). Here, we took a reduced-representation sequencing approach (ddRadSeq and EpiRadSeq) to investigate how CpG site number, as well as resultant DNA methylation, varied across five sites in the [~]70 year-old Kenyan house sparrow range expansion. We found that the number of CpG sites increased towards the vanguard of the invasion, even when accounting for variation in genetic diversity among sites. This pattern was driven by more losses of CpG sites towards the core of the invasion (the initial site of introduction). Across all sequenced loci, DNA methylation decreased but became more variable towards the range-edge. However, in the subset CpG sites proximal to mutated CpG sites, DNA methylation increased and variation declined. These results indicate that epigenetic potential influenced the Kenyan house sparrow range expansion, likely by providing greater phenotypic plasticity which is genetically assimilated as populations adapt to local conditions. Similar mechanisms might underlie the successes and failures of other natural and anthropogenic range expansions.

evolutionary biology↗

Light Pollution Increases West Nile Virus Competence in a Ubiquitous Passerine Reservoir Species

One sentence summaryLight pollution increases host infectiousness.\n\nAbstractLight pollution is a growing problem, but its impacts on infectious disease risk have not been considered. Previous research has revealed that dim light at night (dLAN) dysregulates various immune functions and biorhythms, which hints that dLAN could change the risk of disease epidemics. Here, we demonstrate that dLAN enhances infectiousness of the house sparrow (Passer domesticus), an urban-dwelling avian host of West Nile virus (WNV). Sparrows exposed to dLAN maintained viral titers above the transmission threshold to a biting vector (105 plaque-forming units) for two days longer than controls but did not die at higher rates. A mathematical model revealed that such effects could increase WNV outbreak potential by ~41%. dLAN likely affects other host and vector traits relevant to transmission, so additional research is needed to advise management of zoonotic diseases in light polluted areas.

pathology↗