Abstract

BackgroundAphids are striking in their prodigious reproductive capacity and reliance on microbial endosymbionts, which provision their hosts with necessary amino acids and provide protection against parasites and heat stress. Perhaps as a result of this bacterial dependence, aphids have limited immune function that may leave them vulnerable to bacterial pathogens. An alternative, non-immunological response that may be available to infected aphids is to increase reproduction, thereby ameliorating fitness loss from infection. Such a response would reduce the need to mount a potentially energetically costly immune response, and would parallel that of other hosts that alter life-history traits when there is a risk of infection. Here we examined whether pea aphids (Acyrthosiphon pisum) respond to immunological challenges by increasing reproduction. As a comparison to the response to the internal cue of risk elicited by immunological challenge, we also exposed pea aphids to an external cue of risk - the aphid alarm pheromone (E)-β-farnesene (EBF), which is released in the presence of predators. For each challenge, we also examined whether the presence of symbionts modified the host response, as maintaining host fitness in the face of challenge would benefit both the host and its dependent bacteria.ResultsWe found that aphids stabbed abdominally with a sterile needle had reduced fecundity relative to control aphids but that aphids stabbed with a needle bearing heat-killed bacteria had reproduction intermediate, and statistically indistinguishable, to the aphids stabbed with a sterile needle and the controls. Aphids with different species of facultative symbiotic bacteria had different reproductive patterns overall, but symbionts in general did not alter aphid reproduction in response to bacterial exposure. However, in response to exposure to alarm pheromone, aphids with Hamiltonella defensa or Serratia symbiotica symbiotic infections increased reproduction but those without a facultative symbiont or with Regiella insecticola did not.ConclusionsOverall, our results suggest that pea aphids are able to increase their reproduction in response to specific cues and that symbiont presence sometimes moderates this response. Such increased reproduction in response to risk of death increases the fitness of both aphids and their vertically transmitted symbionts, and since these organisms have high reproductive capacity, slight increases in reproduction could lead to a very large numerical advantage later in the season. Thus both symbiotic partners can benefit by increasing host fecundity under dangerous conditions.

Highlights

  • Aphids are striking in their prodigious reproductive capacity and reliance on microbial endosymbionts, which provision their hosts with necessary amino acids and provide protection against parasites and heat stress

  • Four days after the exposure period ended, when the aphids were nine days old, each aphid was placed onto an individual fava bean sprout in boxes, and fecundity and survival was monitored for six days. We analyzed these data with analyses of variance (ANOVA) with the aphid clone and exposure condition as fixed factors. (2b) Do pea aphids increase reproduction in response to alarm pheromones? Does symbiont presence matter? We explored how symbiont presence altered reproduction when exposed to alarm pheromones by exposing aphids from a clonal line (5A) with each symbiont, H. defensa, R. insecticola, S. symbiotica or no symbiont and a second line (LSR1) with R. insecticola or no symbiont Twenty aphids from each symbiont/line condition were exposed to every challenge

  • While the initial experiments examined how aphids respond to internal cues of mortality risk, we found that external cues of risk alter reproductive responses

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Summary

Introduction

Aphids are striking in their prodigious reproductive capacity and reliance on microbial endosymbionts, which provision their hosts with necessary amino acids and provide protection against parasites and heat stress. Non-immunological response that may be available to infected aphids is to increase reproduction, thereby ameliorating fitness loss from infection. Such a response would reduce the need to mount a potentially energetically costly immune response, and would parallel that of other hosts that alter life-history traits when there is a risk of infection. Investing in an immune response will both reduce immediate reproduction and lifetime reproduction if the immune response fails to overcome the pathogen, or if the immune response itself is sufficiently damaging to the host. Species that are likely to be outcompeted by conspecifics invest more in reproduction and less in growth than the dominant competitors [21]

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