Abstract
BackgroundThe health and resilience of species in natural environments is increasingly challenged by complex anthropogenic stressor combinations including climate change, habitat encroachment, and chemical contamination. To better understand impacts of these stressors we examined the individual- and combined-stressor impacts of malaria infection, food limitation, and 2,4,6-trinitrotoluene (TNT) exposures on gene expression in livers of Western fence lizards (WFL, Sceloporus occidentalis) using custom WFL transcriptome-based microarrays.ResultsComputational analysis including annotation enrichment and correlation analysis identified putative functional mechanisms linking transcript expression and toxicological phenotypes. TNT exposure increased transcript expression for genes involved in erythropoiesis, potentially in response to TNT-induced anemia and/or methemoglobinemia and caused dose-specific effects on genes involved in lipid and overall energy metabolism consistent with a hormesis response of growth stimulation at low doses and adverse decreases in lizard growth at high doses. Functional enrichment results were indicative of inhibited potential for lipid mobilization and catabolism in TNT exposures which corresponded with increased inguinal fat weights and was suggestive of a decreased overall energy budget. Malaria infection elicited enriched expression of multiple immune-related functions likely corresponding to increased white blood cell (WBC) counts. Food limitation alone enriched functions related to cellular energy production and decreased expression of immune responses consistent with a decrease in WBC levels.ConclusionsDespite these findings, the lizards demonstrated immune resilience to malaria infection under food limitation with transcriptional results indicating a fully competent immune response to malaria, even under bio-energetic constraints. Interestingly, both TNT and malaria individually increased transcriptional expression of immune-related genes and increased overall WBC concentrations in blood; responses that were retained in the TNT x malaria combined exposure. The results demonstrate complex and sometimes unexpected responses to multiple stressors where the lizards displayed remarkable resiliency to the stressor combinations investigated.
Highlights
The health and resilience of species in natural environments is increasingly challenged by complex anthropogenic stressor combinations including climate change, habitat encroachment, and chemical contamination
As summarized in McFarland et al [1], stressors that are characteristic of habitat encroachment, climate change, and chemical contamination are pervasive in western North America and result in concern for endemic reptilian populations
Global transcriptomic expression assays are useful for establishing mechanistic and systems-level toxicological outcomes [10], which we have demonstrated for multiple munitions in an array of species [11,12,13,14,15,16,17,18]
Summary
The health and resilience of species in natural environments is increasingly challenged by complex anthropogenic stressor combinations including climate change, habitat encroachment, and chemical contamination. As summarized in McFarland et al [1], stressors that are characteristic of habitat encroachment, climate change, and chemical contamination are pervasive in western North America and result in concern for endemic reptilian populations. The complex nature of these stressor exposures is a concern for sustaining viable endemic reptile populations, the failure of which could jeopardize range access for military operations and training. Given these challenges, we sought to experimentally evaluate the impact of multiple stressors on the health of a representative Western American reptile species, the Western fence lizard (WFL, Sceloporus occidentalis). Global transcriptomic expression was employed to uncover functional responses underlying critical phenotypic outcomes
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