Determining the Advantages, Costs, and Trade-Offs of a Novel Sodium Channel Mutation in the Copepod Acartia hudsonica to Paralytic Shellfish Toxins (PST).

Tomohiko Ai,Michael Finiguerra,Hans G Dam,David E Avery

doi:10.1371/journal.pone.0130097

Abstract

The marine copepod Acartia hudsonica was shown to be adapted to dinoflagellate prey, Alexandrium fundyense, which produce paralytic shellfish toxins (PST). Adaptation to PSTs in other organisms is caused by a mutation in the sodium channel. Recently, a mutation in the sodium channel in A. hudsonica was found. In this study, we rigorously tested for advantages, costs, and trade-offs associated with the mutant isoform of A. hudsonica under toxic and non-toxic conditions. We combined fitness with wild-type: mutant isoform ratio measurements on the same individual copepod to test our hypotheses. All A. hudsonica copepods express both the wild-type and mutant sodium channel isoforms, but in different proportions; some individuals express predominantly mutant (PMI) or wild-type isoforms (PWI), while most individuals express relatively equal amounts of each (EI). There was no consistent pattern of improved performance as a function of toxin dose for egg production rate (EPR), ingestion rate (I), and gross growth efficiency (GGE) for individuals in the PMI group relative to individuals in the PWI expression group. Neither was there any evidence to indicate a fitness benefit to the mutant isoform at intermediate toxin doses. No clear advantage under toxic conditions was associated with the mutation. Using a mixed-diet approach, there was also no observed relationship between individual wild-type: mutant isoform ratios and among expression groups, on both toxic and non-toxic diets, for eggs produced over three days. Lastly, expression of the mutant isoform did not mitigate the negative effects of the toxin. That is, the reductions in EPR from a toxic to non-toxic diet for copepods were independent of expression groups. Overall, the results did not support our hypotheses; the mutant sodium channel isoform does not appear to be related to adaptation to PST in A. hudsonica. Other potential mechanisms responsible for the adaptation are discussed.

Highlights

Evolutionary adaptation to a stressor involves selection for phenotypes that confer a fitness advantage in the presence of the stressor
The relationships between ingestion rate (Fig 1), egg production rate (Fig 2), and gross growth efficiency (Fig 3) and toxin dose as a function of sodium channel expression group, the reaction norms of ingestion, were complex
In the absence of toxins the PWI expression group showed a lower ingestion rate compared to the predominantly mutant (PMI) and EI expression groups (Fig 1; Dunn’s Method p

Summary

Introduction

Evolutionary adaptation to a stressor involves selection for phenotypes that confer a fitness advantage in the presence of the stressor. Adapted phenotypes may pay a fitness cost compared to susceptible phenotypes in the absence of the stressor, because resources allocated to adaptation detract from the overall fitness of an organism [1, 2]. Adaptation to the toxic metal cadmium in Drosophila melanogaster has clear fitness costs and advantages. Cadmium-resistant flies had higher fecundity in a cadmium contaminated environment, an advantage over susceptible flies, but lower fecundity in the absence of cadmium compared to susceptible flies, a cost [3]. A specific phenotype (e.g., resistant) may experience a change in fitness across an environmental gradient, i.e. a trade-off; resistant flies suffered a decrease in fecundity going from an unpolluted to polluted environment. Understanding the advantages, costs, and trade-offs of adaptation is necessary for predicting how a population will respond to a stressor

Methods

Results

Conclusion