Abstract
BackgroundIn cnidarians, antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive. The potentially high cost of venom production has been hypothesized to drive population-specific variation in venom expression due to differences in abiotic conditions. However, the effects of environmental factors on venom production have been rarely demonstrated in animals. Here, we explore the impact of specific abiotic stresses on venom production of distinct populations of the sea anemone Nematostella vectensis (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely.ResultsWe challenged Nematostella polyps with heat, salinity, UV light stressors, and a combination of all three factors to determine how abiotic stressors impact toxin expression for individuals collected across this species’ range. Transcriptomics and proteomics revealed that the highly abundant toxin Nv1 was the most downregulated gene under heat stress conditions in multiple populations. Physiological measurements demonstrated that venom is metabolically costly to produce. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate differently their venom production levels.ConclusionsWe demonstrate that abiotic stress results in venom regulation in Nematostella. Together with anecdotal observations from other cnidarian species, our results suggest this might be a universal phenomenon in Cnidaria. The decrease in venom production under stress conditions across species coupled with the evidence for its high metabolic cost in Nematostella suggests downregulation of venom production under certain conditions may be highly advantageous and adaptive. Furthermore, our results point towards local adaptation of this mechanism in Nematostella populations along a latitudinal cline, possibly resulting from distinct genetics and significant environmental differences between their habitats.
Highlights
In cnidarians, antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive
To confirm that the elevated metabolic rate involved the biosynthesis of venom, we repeated the venom depletion treatment and measured expression levels of genes encoding toxins produced by both adult males and females, nematocyst structural proteins, genes involved in general stress responses, and several housekeeping proteins by nCounter technology (Additional file 1: Data S2)
The investment of energy into heat response appears to be traded-off with other high-cost physiological processes that do not contribute to survival under heat stress
Summary
Antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive. We explore the impact of specific abiotic stresses on venom production of distinct populations of the sea anemone Nematostella vectensis (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely. Nematostella vectensis is a burrowing sea anemone which specializes in estuarine environments with a unique role as an infaunal predator [1]. These brackish habitats are characterized by variable daily and seasonal abiotic conditions, temperature, salinity, and ultraviolet (UV) light [2,3,4,5,6]. The combination of geographically structured genetic variation and differences in environmental conditions is the context where we may expect that populations might be adapted to different ranges of environmental parameters [8, 10, 11]
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