Aphid reproductive investment in response to mortality risks

Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA 30322, USA.
BMC Evolutionary Biology (Impact Factor: 3.37). 08/2010; 10(1):251. DOI: 10.1186/1471-2148-10-251
Source: PubMed


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. 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.
We 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.
Overall, 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.

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    • "Such a failed infection may alert hosts to the presence of a parasite in addition to further cues of an impending attack, for example, through long-term or induced cues. This exposure of the host to the parasite can inform the host to alter reproductive investment in anticipation of possible attack (Minchella and Loverde 1981; Blair and Webster 2007; Barribeau et al. 2010). Here we build on resource allocation models used in van Baalen (1998), Gandon et al. (2002), and Bonds (2006) and separate the events of parasite attack and establishment of infection. "
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    ABSTRACT: Abstract Individuals invest limited resources across vital tasks such as reproduction and survival. Individuals can spread reproductive investment over their lifetime, but cues of death or reduced fitness can influence this investment. In some systems, cues of infection induce early but costly reproduction through fecundity compensation as future reproduction becomes uncertain. A key aspect of parasite biology is the delay between exposure to parasites and the onset of virulence. This creates an important window of opportunity for hosts to respond to infection. Existing models have not accounted for this delay or the costs borne by offspring. We combine a theoretical and experimental approach to assess the role of costs and the importance of delay in virulence on fecundity compensation. We find that a delay in virulence selects for plastic fecundity responses even with moderate offspring costs. We tested our model experimentally by exposing pea aphids, Acyrthosiphon pisum, to various ecologically relevant cues of infection and monitored lifetime reproduction and survival of these aphids and their offspring. Our challenges induced fecundity compensation, but we did not detect any costs in mothers or offspring. We predict that the relationship between the costs and the delay in onset of virulence, as found here, determines the success of fecundity compensation as an adaptation against parasitism.
    The American Naturalist 04/2014; 183(4):480-493. DOI:10.1086/675242 · 3.83 Impact Factor
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    • "While this does not preclude the possibility of such a response in other aphid genotypes or in response to other aphid bacterial pathogens, it does suggest that winged offspring production is not a general response to bacterial invasion. Previous work has shown that at least some aphids, including LSR1, increase the rate of reproduction after pathogen exposure, a mechanism of defense known as fecundity compensation [17,37]. Though our experiment was not designed to test for fecundity compensation, our results were consistent with previous findings; namely, we saw a trend for an increased rate of reproduction in response to exposure to bacterial elicitors relative to a sterile stab (data not shown). "
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    ABSTRACT: Pea aphids have an obligate nutritional symbiosis with the bacteria Buchneraaphidicola and frequently also harbor one or more facultative symbionts. Aphids are also susceptible to bacterial pathogen infections, and it has been suggested that aphids have a limited immune response towards such pathogen infections compared to other, more well-studied insects. However, aphids do possess at least some of the genes known to be involved in bacterial immune responses in other insects, and immune-competent hemocytes. One possibility is that immune priming with microbial elicitors could stimulate immune protection against subsequent bacterial infections, as has been observed in several other insect systems. To address this hypothesis we challenged aphids with bacterial immune elicitors twenty-four hours prior to live bacterial pathogen infections and then compared their survival rates to aphids that were not pre-exposed to bacterial signals. Using two aphid genotypes, we found no evidence for immune protection conferred by immune priming during infections with either Serratia marcescens or with Escherichia coli. Immune priming was not altered by the presence of facultative, beneficial symbionts in the aphids. In the absence of inducible immune protection, aphids may allocate energy towards other defense traits, including production of offspring with wings that could escape deteriorating conditions. To test this, we monitored the ratio of winged to unwinged offspring produced by adult mothers of a single clone that had been exposed to bacterial immune elicitors, to live E. coli infections or to no challenge. We found no correlation between immune challenge and winged offspring production, suggesting that this mechanism of defense, which functions upon exposure to fungal pathogens, is not central to aphid responses to bacterial infections.
    PLoS ONE 08/2013; 8(8):e73600. DOI:10.1371/journal.pone.0073600 · 3.23 Impact Factor
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    • "possible (Ebert et al., 2004; Chadwick & Little, 2005). Life-history shifts maximizing early reproduction, termed fecundity compensation, have been described in several host–parasite systems (Minchella & Loverde, 1981; Thornhill et al., 1986; Krist, 2001; Ebert et al., 2004; Chadwick & Little, 2005; Altincicek et al., 2008; Barribeau et al., 2010). "
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    ABSTRACT: Hosts are armed with several lines of defence in the battle against parasites: they may prevent the establishment of infection, reduce parasite growth once infected or persevere through mechanisms that reduce the damage caused by infection, called tolerance. Studies on tolerance in animals have focused on mortality, and sterility tolerance has not been investigated experimentally. Here, we tested for genetic variation in the multiple steps of defence when the invertebrate Daphnia magna is infected with the sterilizing bacterial pathogen Pasteuria ramosa: anti-infection resistance, anti-growth resistance and the ability to tolerate sterilization once infected. When exposed to nine doses of a genetically diverse pathogen inoculum, six host genotypes varied in their average susceptibility to infection and in their parasite loads once infected. How host fecundity changed with increasing parasite loads did not vary between genotypes, indicating that there was no genetic variation for this measure of fecundity tolerance. However, genotypes differed in their level of fecundity compensation under infection, and we discuss how, by increasing host fitness without targeting parasite densities, fecundity compensation is consistent with the functional definition of tolerance. Such infection-induced life-history shifts are not traditionally considered to be part of the immune response, but may crucially reduce harm (in terms of fitness loss) caused by disease, and are a distinct source of selection on pathogens.
    Journal of Evolutionary Biology 06/2012; 25(9-in press.). DOI:10.1111/j.1420-9101.2012.02579.x · 3.23 Impact Factor
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