Selection on innate immunity and body condition in Florida scrub-jays throughout an epidemic

Opportunities to investigate selection in free-living species during a naturally occurring epidemic are rare; however, we assessed innate immunocompetence in Florida scrub-jays before the population suffered the greatest over-winter mortality in 20 years of study. Propitiously, three months prior to the epidemic, we had sampled a number of male breeders to evaluate a suite of physiological measures that are commonly used to estimate the overall health-state of an individual. There was a significant, positive selection gradient for both Escherichia coli bacterial killing capability and body condition, suggesting that directional selection had occurred upon each of these traits during the disease epidemic.     

A test of life-history theories of immune defence in two ecotypes of the garter snake, Thamnophis elegans

1.  Life-history theorists have long observed that fast growth and high reproduction tend to be associated with short life span, suggesting that greater investment in such traits may trade off with self-maintenance. The immune system plays an integral role in self-maintenance and has been proposed as a mediator of life-history trade-offs.
2.  Ecoimmunologists have predicted that fast-living organisms should rely more heavily on constitutive innate immunity than slow-living organisms, as constitutive innate defences are thought to be relatively inexpensive to develop and can provide a rapid, general response to pathogens.
3.  We present the first study to examine this hypothesis in an ectothermic vertebrate, by testing for differences in three aspects of constitutive innate immunity in replicate populations of two life-history ecotypes of the garter snake Thamnophis elegans , one fast-living and one slow-living.
4.  As predicted, free-ranging snakes from the fast-living ecotype had higher levels of all three measures of constitutive innate immunity than the slow-living ecotype. These differences in immunity were not explained by parasite loads measured. Furthermore, both ecotypes exhibited a positive relationship between innate immunity and body size/age, which we discuss in the context of ectotherm physiology and ecotype differences in developmental rates.     

A carbohydrate-rich diet increases social immunity in ants

Increased potential for disease transmission among nest-mates means living in groups has inherent costs. This increased potential is predicted to select for disease resistance mechanisms that are enhanced by cooperative exchanges among group members, a phenomenon known as social immunity. One potential mediator of social immunity is diet nutritional balance because traits underlying immunity can require different nutritional mixtures. Here, we show how dietary protein–carbohydrate balance affects social immunity in ants. When challenged with a parasitic fungus Metarhizium anisopliae, workers reared on a high-carbohydrate diet survived approximately 2.8× longer in worker groups than in solitary conditions, whereas workers reared on an isocaloric, high-protein diet survived only approximately 1.3× longer in worker groups versus solitary conditions. Nutrition had little effect on social grooming, a potential mechanism for social immunity. However, experimentally blocking metapleural glands, which secrete antibiotics, completely eliminated effects of social grouping and nutrition on immunity, suggesting a causal role for secretion exchange. A carbohydrate-rich diet also reduced worker mortality rates when whole colonies were challenged with Metarhizium. These results provide a novel mechanism by which carbohydrate exploitation could contribute to the ecological dominance of ants and other social groups.     

A genetics‐based approach confirms immune associations with life history across multiple populations of an aquatic vertebrate (Gasterosteus aculeatus)

Understanding how wild immune variation covaries with other traits can reveal how costs and trade‐offs shape immune evolution in the wild. Divergent life history strategies may increase or alleviate immune costs, helping shape immune variation in a consistent, testable way. Contrasting hypotheses suggest that shorter life histories may alleviate costs by offsetting them against increased mortality, or increase the effect of costs if immune responses are traded off against development or reproduction. We investigated the evolutionary relationship between life history and immune responses within an island radiation of three‐spined stickleback, with discrete populations of varying life histories and parasitism. We sampled two short‐lived, two long‐lived and an anadromous population using qPCR to quantify current immune profile and RAD‐seq data to study the distribution of immune variants within our assay genes and across the genome. Short‐lived populations exhibited significantly increased expression of all assay genes, which was accompanied by a strong association with population‐level variation in local alleles and divergence in a gene that may be involved in complement pathways. In addition, divergence around the eda gene in anadromous fish is likely associated with increased inflammation. A wider analysis of 15 populations across the island revealed that immune genes across the genome show evidence of having diverged alongside life history strategies. Parasitism and reproductive investment were also important sources of variation for expression, highlighting the caution required when assaying immune responses in the wild. These results provide strong, gene‐based support for current hypotheses linking life history and immune variation across multiple populations of a vertebrate model.     

Links between blood parasites,blood chemistry,and the survival of nestling American crows

Many studies have used the avian hemosporidians (Leucocytozoon, Plasmodium, and Hemoproteus) to test hypotheses of host–parasite co‐evolution, yet documented health and survival consequences of these blood parasites vary among studies and generalizations about their pathogenicity are debatable. In general, the negative effects of the hemosporidians are likely to be greatest during acute infections of young birds, yet most previous studies in wild passerines have examined chronic effects in adults. Here, we evaluated responses of nestling American crows (Corvus brachyrhynchos) to acute infection (prevalence and burden), as well as its short‐ and long‐term survival consequences. We used panel of nine hematological and biochemical parameters that are regularly used to evaluate the health of domestic animals, including leukocyte profiles, hematocrit, and plasma proteins. We assessed the effects of infection on survival in a mark‐recapture framework. Overall, 56% of crows (n = 321 samples) were infected by at least one of the three genera. Infections by all genera were associated with elevated plasma proteins and globulins, which could indicate an adaptive immune response. However, only Plasmodium infections were associated with low hematocrit (anemia) and lower fledging success, possibly mediated by the negative effect of low hematocrit values on body condition. Moreover, early Plasmodium infection (<40 days of age) had long‐term survival implications: it was associated with lower apparent survival probability within 3 years after fledging. These results suggest that young crows mounted an adaptive immune response to all three genera. Short‐ and long‐term pathological effects, however, were only apparent with Plasmodium infections.     

Ontogenetic changes in innate immune function in captive and wild subspecies of prairie-chickens (Tympanuchus cupido spp.)

The Attwater's prairie-chicken (Tympanuchus cupido attwateri), a federally endangered grouse species, is currently experiencing high chick mortality in wild populations and the causes are unknown. We tested 3 indicators of innate immunity (hemaggluttination, serum lysozyme, and total immunoglobulin [IgY] levels) in the Attwater's prairie-chicken and a closely related sub-species, the greater prairie-chicken (Tympanuchus cupido pinnatus). Agglutination titers were approximately 25% higher in the juvenile and adult Attwater's prairie-chickens compared to equivalently aged greater prairie-chickens. Additionally, total IgY levels in wild-collected Attwater's prairie-chicken egg samples were 34% higher than IgY levels in captive greater prairie-chickens or Attwater's prairie-chicken eggs. These results suggest that differences in innate immune function exist between these sub-species and also among Attwater's prairie-chicken subpopulations that are exposed to different environmental conditions. © 2012 The Wildlife Society.     

Experimental demonstration of a parasite‐induced immune response in wild birds: Darwin's finches and introduced nest flies

Ecological immunology aims to explain variation among hosts in the strength and efficacy of immunological defenses. However, a shortcoming has been the failure to link host immune responses to actual parasites under natural conditions. Here, we present one of the first experimental demonstrations of a parasite‐induced immune response in a wild bird population. The recently introduced ectoparasitic nest fly Philornis downsi severely impacts the fitness of Darwin's finches and other land birds in the Galápagos Islands. An earlier study showed that female medium ground finches (Geospiza fortis) had P. downsi‐binding antibodies correlating with presumed variation in fly exposure over time. In the current study, we experimentally manipulated fly abundance to test whether the fly does, in fact, cause changes in antibody levels. We manipulated P. downsi abundance in nests and quantified P. downsi‐binding antibody levels of medium ground finch mothers, fathers, and nestlings. We also quantified host behaviors, such as preening, which can integrate with antibody‐mediated defenses against ectoparasites. Philornis downsi‐binding antibody levels were significantly higher among mothers at parasitized nests, compared to mothers at (fumigated) nonparasitized nests. Mothers with higher antibody levels tended to have fewer parasites in their nests, suggesting that antibodies play a role in defense against parasites. Mothers showed no behavioral changes that would enhance the effectiveness of the immune response. Neither adult males, nor nestlings, had P. downsi‐induced immunological or behavioral responses that would enhance defense against flies. None of the parasitized nests fledged any offspring, despite the immune response by mothers. Thus, this study shows that, while the immune response of mothers appeared to be defensive, it was not sufficient to rescue current reproductive fitness. This study further shows the importance of testing the fitness consequences of immune defenses, rather than assuming that such responses increase host fitness.     

Male chemical cues as reliable indicators of infection in the wolf spider Schizocosa ocreata

Sexual signals can convey important information about mate quality, such as critical information about a signaler's health status, helping an individual to avoid infected or immunocompromised conspecifics. Chemical signals are especially important in this context, because they represent an honest and dynamic signaling modality that receivers can use to make updated mate choice decisions to avoid compromising their own health. In this study, we investigated the viability of male chemical cues in the wolf spider Schizocosa ocreata as a reliable indicator of health status. Using video playback with images of an average male that is simultaneously paired with male cuticular compounds on filter paper, we show that females are more receptive to videos paired with cues from control males rather than infected males. We also show that these cuticular compounds can be isolated and retain similar female behavioral responses when extracted with a nonpolar solvent, suggesting that these cuticular compounds may not be just complex hydrocarbons, but a combination of cuticular compounds. This is the first evidence for female discrimination and recognition of male chemical cues in this species, which opens up important new avenues of research in a well‐studied species with complex multimodal signaling.     

Bighorn sheep show similar in‐host responses to the same pathogen strain in two contrasting environments

Ecological context—the biotic and abiotic environment, along with its influence on population mixing dynamics and individual susceptibility—is thought to have major bearing on epidemic outcomes. However, direct comparisons of wildlife disease events in contrasting ecological contexts are often confounded by concurrent differences in host genetics, exposure histories, or pathogen strains. Here, we compare disease dynamics of a Mycoplasma ovipneumoniae spillover event that affected bighorn sheep populations in two contrasting ecological contexts. One event occurred on the herd''s home range near the Rio Grande Gorge in New Mexico, while the other occurred in a captive facility at Hardware Ranch in Utah. While data collection regimens varied, general patterns of antibody signal strength and symptom emergence were conserved between the two sites. Symptoms appeared in the captive setting an average of 12.9 days postexposure, average time to seroconversion was 24.9 days, and clinical signs peaked at approximately 36 days postinfection. These patterns were consistent with serological testing and subsequent declines in symptom intensity in the free‐ranging herd. At the captive site, older animals exhibited more severe declines in body condition and loin thickness, higher symptom burdens, and slower antibody response to the pathogen than younger animals. Younger animals were more likely than older animals to clear infection by the time of sampling at both sites. The patterns presented here suggest that environment may not be a major determinant of epidemiological outcomes in the bighorn sheep—M. ovipneumoniae system, elevating the possibility that host‐ or pathogen‐factors may be responsible for observed variation.