Search bioRxiv⌕ Search

Biology subjects

Fleming-Davies, A.

Publications and source records attributed to Fleming-Davies, A..

6 recordsLinked to original sources

Immediate and carryover reproductive costs of infection in female but not male house finches

Wildlife diseases cause well-documented and often dramatic reductions in host survival. However, the impact of infectious diseases on host reproduction remains understudied, especially with respect to effects of prior and/or current pathogen exposure on reproductive development. Here we experimentally tested how prior and/or current infection with a common bacterial pathogen, Mycoplasma gallisepticum ( MG), alters reproductive development for female versus male house finches (Haemorhous mexicanus). Finches were inoculated with either MG or sterile media while in wintering condition and subsequently received one of these treatments while in breeding condition. In females, MG exposure had both immediate and carry-over effects on reproduction: controls had higher odds of laying eggs compared to females inoculated with MG in spring only, higher odds than females inoculated in both winter and spring, and higher odds than females given MG in the winter only. Conversely, breeding-condition males inoculated with MG in spring had higher testosterone levels than males receiving only control inoculations, and there were no carryover effects of winter MG inoculation or inoculations during both seasons on testosterone. Sex bias in the reproductive impacts of infectious diseases may have important knock-on effects on the epidemiology and population-regulating effects of pathogens, thereby warranting further study.

ecology↗

Wandering the NPV Maze: Nucleopolyhedrovirus infection alters Gulf Fritillary (Dione vanillae) larval wandering behavior

Parasites can manipulate host behavior to increase their fitness while decreasing host fitness, a phenomenon known as an extended phenotype. Nucleopolyhedroviruses (NPVs), baculoviruses that infect Lepidopteran larvae, have been found to induce vertical climbing behavior and hyperactivity in exposed larvae. We quantified variation in the horizontal wandering behavior induced by different naturally-occurring pathogen isolates in the NPV that infects Dione (Agraulis) vanillae Linnaeus (Lepidoptera: Nymphalidae). Lab-raised larvae were infected with a constant dose of one of five different field-collected NPV isolates or a water control (n=97 larvae total), and placed in mazes to measure the horizontal distance wandered away from a food source. Virus-exposed larvae exhibited increased maximum distance of horizontal movement compared to the control, but did not significantly differ in the probability of wandering versus no movement. We also found variation in the distance wandered among the five virus isolates. However, grouping the five isolates into two previously-described viral strains or genogroups did not improve predicted differences in movement, perhaps due to the presence of within-strain genetic variation among isolates in the viral genes involved in controlling host behavior. Further work is needed to determine whether the observed between-isolate variation is the result of adaptive evolution. These results suggest that the NPV infecting D. vanillae manipulates larval behavior to increase horizontal wandering, which could lead to higher pathogen fitness by increasing long-distance dispersal of the virus across the landscape.

ecology↗

Paying upfront: successful initial infections protect against severe future infections

Understanding the consistency with which individual hosts respond to repeated pathogen exposures is crucial for accurately modeling pathogen transmission and eco-evolutionary dynamics. When hosts face repeated pathogen exposures, immune memory is expected to reduce the probability and/or severity of subsequent infections, yet it remains unclear whether individuals remain consistent in their level of response relative to others. We investigated this question in house finches (Haemorhous mexicanus) from two populations varying in history of endemism of the bacterial pathogen Mycoplasma gallisepticum (MG). Individuals were confirmed to be MG-naive at capture and then experimentally inoculated twice with MG, allowing recovery between inoculations. We then asked if host responses to the second inoculation were predicted by responses to initial inoculation, sex, or population of origin. Our results suggest that individuals were not consistent in their relative response levels; rather, a successful initial infection provided protection against a severe second infection, increasing both tolerance and resistance. While we found no population differences in response to the second inoculation, males showed higher susceptibility to the second inoculation than females. Investigating and accounting for individual variation in response to subsequent exposures may improve the precision and accuracy of transmission models for wildlife pathogens.

ecology↗

Infected host competence overshadows heterogeneity in susceptibility in shaping experimental epizootics

The accelerated rate of disease emergence in recent decades underscores the need to understand conditions that promote or dampen epidemics. Theoretical models consistently show that epidemics are smaller in populations with higher among-individual heterogeneity in susceptibility. Experimental tests of these predictions are rare but critical for understanding how heterogeneity in susceptibility shapes epidemics in natural systems. We directly link data-parameterized models from previous dose response experiments in the house finch and Mycoplasma gallisepticum system to experimental epidemics in replicated aviary mesocosm flocks. We manipulated flock-level heterogeneity in susceptibility by seeding epidemics in flocks composed of either pathogen-naive or previously exposed birds, which prior work showed have higher heterogeneity in susceptibility relative to pathogen-naive populations. We tracked epidemics for over two months, combining empirical data and stochastic compartmental models to address how heterogeneity in susceptibility changes epidemic severity. Consistent with previous work, estimates of heterogeneity in susceptibility based on coefficients of variation were higher for flocks given prior pathogen exposure relative to pathogen-naive flocks. However, in contrast with prior work on individually-housed birds which showed relatively homogeneous susceptibility for pathogen-naive birds, the pathogen-naive flocks in this study were better described by heterogeneous, rather than homogenous, models of susceptibility. This suggests that flock-level epidemics captured sources of heterogeneity absent in controlled experiments, such as transmission heterogeneity. Finally, although prior exposure conferred protection from disease at the individual level, we did not detect predicted effects of prior exposure and its associated flock-level heterogeneity on prevalence. However, our ability to detect effects of prior exposure on flock-level prevalence was obscured by unexpected variation in the competence of the initially pathogen-naive index birds that seeded each epidemic. This variation in infectiousness among index birds significantly predicted flock-level prevalence, with low index bird infectiousness contributing to the absence of detectable epidemics in two of the three naive flocks. Our stochastic simulations generated a wide range of prevalence outcomes for small epidemics over the timescales examined, further underscoring the challenges of measuring transmission dynamics in naturalistic settings, where unexpected variation in host traits such as competence can obscure other factors of interest. Open research statementData are not yet provided. Data and code will be permanently and publicly archived in the Virginia Tech Data Repository if the paper is accepted for publication

ecology↗

Pathogen priming alters host transmission potential and predictors of transmissibility in a wild songbird species

Pathogen reinfections occur widely, but the extent to which reinfected hosts contribute to ongoing transmission is often unknown despite its implications for host-pathogen dynamics. House finches (Haemorhous mexicanus) acquire partial protection from initial exposure to the bacterial pathogen Mycoplasma gallisepticum (MG), with hosts readily reinfected with homologous or heterologous strains on short timescales. However, the extent to which reinfected hosts contribute to MG transmission has not been tested. We used three pathogen priming treatments- none, intermediate (repeated low-dose priming), or high (single high-dose priming)- to test how prior pathogen priming alters the likelihood of transmission to a cagemate during index bird reinfection with a homologous or heterologous MG strain. Relative to unprimed control hosts, the highest priming level strongly reduced maximum pathogen loads and transmission success of index birds during reinfections. Reinfections with the heterologous strain, previously shown to be more virulent and transmissible than the homologous strain used, resulted in higher pathogen loads within high-primed index birds, and showed higher overall transmission success regardless of host priming treatment. This suggests that inherent differences in strain transmissibility are maintained in primed hosts, leading to the potential for ongoing transmission during reinfections. Finally, among individuals, transmission was most likely from hosts harboring higher within-host pathogen loads, while associations between disease severity and transmission probability were dependent on a given birds priming treatment. Overall, our results indicate that reinfections can result in ongoing transmission, particularly where reinfections result from heterologous and highly transmissible strains, with key implications for virulence evolution. ImportanceAs Covid-19 dramatically illustrated, humans and other animals can become infected with the same pathogen multiple times. Because individuals already have defenses against pathogen their immune systems have encountered before, reinfections are typically less severe, and are thought to be less contagious, but this is rarely directly tested. We used a songbird species and two strains of its common bacterial pathogen to study how contagious hosts are when their immune systems have some degree of prior experience with a pathogen. We found that reinfected hosts are not as contagious as initially infected ones. However, the more transmissible of the two strains, which also causes more harm to its hosts, was able to multiply more readily than the other strain within reinfected hosts, and was more contagious in both reinfected and first-infected hosts. This suggests that reinfections might favor more harmful pathogen strains that are better able to overcome immune defenses.

evolutionary biology↗

Eco-evolutionary theory and insect outbreaks

Eco-evolutionary theory argues that population cycles in consumer-resource interactions are partly driven by natural selection, such that changes in densities and changes in trait values are mutually reinforcing. Evidence that this theory explains cycles in nature, however, is almost nonexistent. Experimental tests of model predictions are almost always impossible because of the long time scales over which cycles occur, but for most organisms, even tests of model assumptions are logistically impractical. For insect baculoviruses in contrast, tests of model assumptions are straightforward, and baculoviruses often drive outbreaks of forest-defoliating insects, as in the gypsy moth that we study here. We therefore used field experiments with the gypsy moth baculovirus to test two key assumptions of eco-evolutionary models of host-pathogen population cycles, that reduced host infection risk is heritable and costly. Our experiments confirm the two assumptions, and inserting parameters estimated from our data into the models gives cycles closely resembling gypsy moth outbreak cycles in North America, whereas standard models predict unrealistic stable equilibria. Our work shows that eco-evolutionary models are useful for explaining outbreaks of forest insect defoliators, while widespread observations of intense selection imposed by natural enemies on defoliators, and frequent laboratory observations of heritable and costly resistance in defoliators, suggest that eco-evolutionary dynamics may play a general role in defoliator outbreaks.

ecology↗