Exposure to stressors over prolonged periods can have fitness‐relevant consequences, including suppression of immune function. We tested for effects of presence of an invasive species threat on a broad panel of immune functions of a coexisting lizard. Eastern fence lizards (
On exposure to stressors, energy is diverted from non-urgent functions towards those important for immediate survival. The degree and nature of reallocation may be affected by the evolutionary history of the animal. The eastern fence lizard (Sceloporus undulatus) coexists in parts of its range with invasive fire ants (Solenopsis invicta), which attack and wound lizards and elevate stress-relevant hormones (corticosterone), whereas other populations have never been exposed to fire ants. We examined how a history of fire ant invasion affected the immune response in female lizards after exposure to exogenous corticosterone (mimicking exposure to a stressor) during gestation (dosing regimens differed among corticosterone-exposed lizards owing to the constraints of the original studies, but we found no evidence that this affected the outcome of the present study). A history of exposure to predatory stressors (fire ants) and corticosterone treatment affected cell-mediated immunity. Lizards from fire ant-invaded sites had a reduced immune response compared with those from uninvaded sites. Corticosterone treatment had no effect on the immune response of lizards from invaded sites but reduced the immune response of lizards from uninvaded sites. This suggests that an evolutionary history of exposure to wounding alters the immune response to corticosterone. Future work on how the immune system responds to environmental threats will be informative for the prediction and management of these threats.
more » « less- NSF-PAR ID:
- 10121774
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Biological Journal of the Linnean Society
- ISSN:
- 0024-4066
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Sceloporus undulatus ) have been exposed to invasive fire ants (Solenopsis invicta ) for over 80 years. Fire ants sting and envenomate lizards, causing physiological stress, but we do not have a comprehensive understanding of the broad immune consequences of lizard exposure to fire ant presence. We conducted a suite of immune measures on fence lizards caught from areas with long histories of fire ant invasion and lizards from areas not yet invaded by fire ants. The effect of fire ant presence on immunity varied depending on the immune component measured: within fire ant invaded areas, some portions of immunity were suppressed (lymphocytic cell‐mediated immunity, complement), some were unaffected (phagocytic respiratory burst, natural antibodies), and some were enhanced (anti‐fire ant immunoglobulin M, basophils) compared to within uninvaded areas. Rather than fire ants being broadly immunosuppressing, as generally assumed, the immune response appears to be tailored to this specific stressor: the immune measures that were enhanced are important to the lizards' ability to handle envenomation, whereas those that were unaffected or suppressed are less critical to surviving fire ant encounters. Several immune measures were suppressed in reproductive females when actively producing follicles, which may make them more susceptible to immunosuppressive costs of stressors such as interactions with fire ants. -
more » « less
Abstract Understanding the processes driving formation and maintenance of latitudinal clines has become increasingly important in light of accelerating global change. Many studies have focused on the role of abiotic factors, especially temperature, in generating clines, but biotic factors, including the introduction of non‐native species, may also drive clinal variation. We assessed the impact of invasion by predatory fire ants on latitudinal clines in multiple fitness‐relevant traits—morphology, physiological stress responsiveness, and antipredator behavior—in a native fence lizard. In areas invaded by fire ants, a latitudinal cline in morphology is opposite both the cline found in museum specimens from historical populations across the species’ full latitudinal range and that found in current populations uninvaded by fire ants. Similarly, clines in stress‐relevant hormone response to a stressor and in antipredator behavior differ significantly between the portions of the fence lizard range invaded and uninvaded by fire ants. Changes in these traits within fire ant‐invaded areas are adaptive and together support increased and more effective antipredator behavior that allows escape from attacks by this invasive predator. However, these changes may mismatch lizards to the environments under which they historically evolved. This research shows that novel biotic pressures can alter latitudinal clines in multiple traits within a single species on ecological timescales. As global change intensifies, a greater understanding of novel abiotic and biotic pressures and how affected organisms adapt to them across space and time will be central to predicting and managing our changing environment.
-
Abstract It is frequently hypothesized that animals employ a generalized “stress response,” largely mediated by glucocorticoid (GC) hormones, such as corticosterone, to combat challenging environmental conditions. Under this hypothesis, diverse stressors are predicted to have concordant effects across biological levels of an organism. We tested the generalized stress response hypothesis in two complementary experiments with juvenile and adult male Eastern fence lizards (Sceloporus undulatus). In both experiments, animals were exposed to diverse, ecologically-relevant, acute stressors (high temperature or red imported fire ants, Solenopsis invicta) and we examined their responses at three biological levels: behavioral; physiological (endocrine [plasma corticosterone and blood glucose concentrations] and innate immunity [complement and natural antibodies]); and cellular responses (gene expression of a panel of five heat-shock proteins in blood and liver) at 30 or 90 min post stress initiation. In both experiments, we observed large differences in the cellular response to the two stressors, which contrasts the similar behavioral and endocrine responses. In the adult experiment for which we had innate immune data, the stressors affected immune function independently, and they were correlated with CORT in opposing directions. Taken together, these results challenge the concept of a generalized stress response. Rather, the stress response was context specific, especially at the cellular level. Such context-specificity might explain why attempts to link GC hormones with life history and fitness have proved difficult. Our results emphasize the need for indicators at multiple biological levels and whole-organism examinations of stress.more » « less
-
null (Ed.)Ecological impacts associated with ant introductions have received considerable attention, but most studies that report on these impacts contrast species assemblages between invaded and uninvaded sites. Given the low inferential power of this type of space-for-time comparison, alternative approaches are needed to evaluate claims that ant invasions drive native species loss. Here, we use long-term data sets from two different Argentine ant eradication programs on the California Channel Islands to examine how the richness and composition of native ant assemblages change before and after invasion (but prior to the initiation of treatments). At four different sites on two different islands, pre-invasion native ant assemblages closely resembled those at uninvaded (control) sites in terms of species richness, species composition, and the presence of multiple indicator species. Invader arrival coincided with large (> 75%) and rapid (within 1 year) declines in species richness, shifts in species composition, and the loss of indicator species. These impacts will hopefully be reversed by the recolonization of formerly invaded areas by native ant species following Argentine ant treatment, and long-term studies of native ant recovery at these sites are ongoing. Unchecked spread of the Argentine ant on other islands in this archipelago, however, poses a grave threat to native ants, which include a number of endemic taxa.more » « less
-
more » « less
Abstract When animals are sick, their physiology and behavior change in ways that can impact their offspring. Research is emerging showing that infection risk alone can also modify the physiology and behavior of healthy animals. If physiological responses to environments with high infection risk take place during reproduction, it is possible that they lead to maternal effects. Understanding whether and how high infection risk triggers maternal effects is important to elucidate how the impacts of infectious agents extend beyond infected individuals and how, in this way, they are even stronger evolutionary forces than already considered. Here, to evaluate the effects of infection risk on maternal responses, we exposed healthy female Japanese quail to either an immune-challenged (lipopolysaccharide [LPS] treated) mate or to a healthy (control) mate. We first assessed how females responded behaviorally to these treatments. Exposure to an immune-challenged or control male was immediately followed by exposure to a healthy male, to determine whether treatment affected paternity allocation. We predicted that females paired with immune-challenged males would avoid and show aggression towards those males, and that paternity would be skewed towards the healthy male. After mating, we collected eggs over a 5-day period. As an additional control, we collected eggs from immune-challenged females mated to healthy males. We tested eggs for fertilization status, embryo sex ratio, as well as albumen corticosterone, lysozyme activity, and ovotransferrin, and yolk antioxidant capacity. We predicted that immune-challenged females would show the strongest changes in the egg and embryo metrics, and that females exposed to immune-challenged males would show intermediate responses. Contrary to our predictions, we found no avoidance of immune-challenged males and no differences in terms of paternity allocation. Immune-challenged females laid fewer eggs, with an almost bimodal distribution of sex ratio for embryos. In this group, albumen ovotransferrin was the lowest, and yolk antioxidant capacity decreased over time, while it increased in the other treatments. No differences in albumen lysozyme were found. Both females that were immune-challenged and those exposed to immune-challenged males deposited progressively more corticosterone in their eggs over time, a pattern opposed to that shown by females exposed to control males. Our results suggest that egg-laying Japanese quail may be able to respond to infection risk, but that additional or prolonged sickness symptoms may be needed for more extensive maternal responses.
