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. 2014 Jun 23;9(6):e100163.
doi: 10.1371/journal.pone.0100163. eCollection 2014.

The roles of standing genetic variation and evolutionary history in determining the evolvability of anti-predator strategies

Daniel R O'Donnell  1 , Abhijna Parigi  1 , Jordan A Fish  2 , Ian Dworkin  3 , Aaron P Wagner  4
Affiliations

The roles of standing genetic variation and evolutionary history in determining the evolvability of anti-predator strategies

Daniel R O'Donnell et al. PLoS One. .

Abstract

Standing genetic variation and the historical environment in which that variation arises (evolutionary history) are both potentially significant determinants of a population's capacity for evolutionary response to a changing environment. Using the open-ended digital evolution software Avida, we evaluated the relative importance of these two factors in influencing evolutionary trajectories in the face of sudden environmental change. We examined how historical exposure to predation pressures, different levels of genetic variation, and combinations of the two, affected the evolvability of anti-predator strategies and competitive abilities in the presence or absence of threats from new, invasive predator populations. We show that while standing genetic variation plays some role in determining evolutionary responses, evolutionary history has the greater influence on a population's capacity to evolve anti-predator traits, i.e. traits effective against novel predators. This adaptability likely reflects the relative ease of repurposing existing, relevant genes and traits, and the broader potential value of the generation and maintenance of adaptively flexible traits in evolving populations.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Design of the experiment to test the effects of SGV and EH on evolution of anti-predator traits.
A) 9 identical prey are injected to initialize two sets of 30 base populations. B) Over the course of 2 million updates of evolution, populations diversified, including the de novo evolution of predators in half of these EH populations (top). C) One fully evolved prey population from each EH treatment (with and without evolving predators) was used to create 30 identical sets of high, intermediate, and no diversity (clone) SGV populations (totaling 2×30×3 = 180 populations), with clones of the best evolved predator from Phase 1 added to each. D) After a further 2 million updates of evolution at a low mutation rate, replicate populations converged on an intermediate level of diversity, but SGV and EH differences result in trait variation among populations. E) To evaluate the effectiveness of evolved anti-predator traits, each of the 180 fully evolved populations from D were introduced, in turn, into separate competition assays with one randomly selected replicate from each of the other EH×SGV combination populations, both in the presence and in the absence of a new novel predator. F) Separately, prey rates of executing “anti-predator” actions (moves, turns, looks) were recorded in the presence and absence of predators, to quantify expressed behavioral responses to predators for all fully evolved populations.
Figure 2
Figure 2. Ecological competition.
Populations from all SGV and EH treatment combinations are randomly paired in competition in the absence (gray boxes, above diagonal) and presence (black boxes, below diagonal) of a novel predator (Phase 3). EH had a far greater effect on competitive outcomes than SGV in both the presence and absence of predators, with predator EH populations competitively dominant in most cases. Y-axis: relative abundance of each lineage in competition. Colors for each lineage indicate SGV and EH treatment history. Black: clone, predator; Gray: clone, no predator; Blue: intermediate, predator; Red: intermediate, no predator; Gold: high, predator; Pink: high, no predator. Dots indicate mean relative abundance for lineages of each treatment after 10,000 updates of competition.
Figure 3
Figure 3. Change in total prey instructions executed (start of Phase 2 minus end of Phase 2), reflecting change in gestation time (or lifespan) resulting from Phase 2 evolution.
“Predator present/absent” refers to the presence or absence of a novel predator during trait assays before and after Phase 2 evolution. Total instructions either increased or decreased very little in predator EH populations, and universally decreased in no predator EH populations. Bars are ±95% CI.
Figure 4
Figure 4. Change in (top) prey moves, (middle) prey turns, and (bottom) prey looks as proportions of total prey instructions, resulting from Phase 2 evolution with a novel predator.
“Predator present/absent” refers to the presence/absence of the Phase 3 novel predator during the trait assays. Traits in predator EH populations generally evolved to a greater extent than did traits in no predator EH populations, and traits often evolved in different directions between the two EH treatments. Bars are ±95% CI.
Figure 5
Figure 5. Change in attacks in behavioral assays pairing the Phase 3 predator with pre- and post-Phase 2 prey populations.
Predator attack frequencies on predator EH populations universally decreased, and generally changed more than did attack frequencies on no predator EH populations. Bars are ±95% CI.
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Grants and funding

Funding was provided by BEACON Center for the Study of Evolution in Action (NSF Cooperative Agreement DBI-0939454), beacon-center.org; and Michigan State University Institute for Cyber Enabled Research, icer.msu.edu. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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