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Does getting defensive get you anywhere?--- Seasonally varying selection in pea aphids shapes a dynamic infection polymorphism with a protective bacterial endosymbiont
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  • Drew Smith,
  • Michael O'Connor,
  • Brooke Deal,
  • Coleman Kotzer,
  • Amanda Lee,
  • Barrett Wagner,
  • Jonah Joffe,
  • Stephen Woloszynek,
  • Kerry Oliver,
  • Jacob Russell
Drew Smith
Drexel University
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Michael O'Connor
Drexel University
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Brooke Deal
Drexel University
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Coleman Kotzer
Drexel University
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Amanda Lee
Drexel University
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Barrett Wagner
Drexel University
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Jonah Joffe
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Stephen Woloszynek
Drexel University
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Kerry Oliver
University of Georgia College of Agricultural and Environmental Sciences
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Jacob Russell
Drexel University
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Abstract

Facultative, heritable endosymbionts are found at intermediate prevalence within most insect species, playing frequent roles in their hosts’ defense against environmental pressures. Focusing on Hamiltonella defensa, a common bacterial endosymbiont of aphids, we tested the hypothesis that such pressures impose seasonal balancing selection, shaping a widespread infection polymorphism. In our studied pea aphid (Acyrthosiphon pisum) population, Hamiltonella infection frequencies ranged from 23.2% to 68.1% across a six-month longitudinal survey. Rapid spikes and declines were consistent across fields, and we estimated that selection coefficients, for Hamiltonella-infected aphids, changed sign within this single season. Prior laboratory research suggested anti-parasitoid defense as the major Hamiltonella benefit, and costs under parasitoid absence. While a prior field study supported these forces as counter-weights in a regime of seasonal balancing selection, our present survey showed no significant relationship between parasitoid wasps and Hamiltonella. Field cage experiments provided some explanation: parasitoids drove ~10% boosts to Hamiltonella frequencies that would be hard to detect under less controlled conditions. They also showed that Hamiltonella was not always costly under parasitoid exclusion, contradicting another long-held prediction. Instead, our longitudinal survey – and two overwintering studies - showed temperature to be the strongest predictor of Hamiltonella infection, matching some lab discoveries, and suggesting thermally sensitive costs and benefits, unrelated to parasitism, can shape this symbiont’s prevalence. These results add to a growing body of evidence arguing for rapid, seasonal adaptation in multivoltine organisms. For many insects, such adaptation may be mediated through the diverse impacts of heritable symbionts on host phenotypes.

Peer review status:IN REVISION

29 Jun 2020Submitted to Molecular Ecology
30 Jul 2020Reviewer(s) Assigned
12 Sep 2020Review(s) Completed, Editorial Evaluation Pending
23 Sep 2020Editorial Decision: Revise Minor