Lobesia botrana Larvae Develop Faster in the Presence of Parasitoids

PLOS ONE, Dec 2019

To combat parasitism hosts often rely on their immune system, which is the last line of defense. However, the immune system may not always be effective, and other non-immunological defenses might be favored to reduce the cost of parasite infection. Here we report that larvae of the moth Lobesia botrana can rapidly accelerate their development and reach maturity earlier in response to cues perceived at a distance from parasitoids. Such a phenotypically plastic life history shift, induced by the perception of deadly enemies in the environment, is likely to be an adaptive defensive strategy to prevent parasitoid attack, and has important implications in host–parasite dynamics.

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Lobesia botrana Larvae Develop Faster in the Presence of Parasitoids

Citation: Vogelweith F, Moret Y, Thiery D, Moreau J ( Lobesia botrana Larvae Develop Faster in the Presence of Parasitoids Fanny Vogelweith 0 Yannick Moret 0 Denis Thiery 0 Je ro me Moreau 0 Guy Smagghe, Ghent University, Belgium 0 1 Universite de Bourgogne , Equipe Ecologie Evolutive, UMR 6282 Bioge osciences, Dijon , France , 2 INRA UMR 1065 Sante et Agroecologie du Vignoble, Institut des Science de la Vigne et du Vin, Villenave d'Ornon Cedex, France, 3 Universite de bordeaux, INRA UMR 1065, Save , Bordeaux Sciences Agro, Villenave d'Ornon Cedex , France To combat parasitism hosts often rely on their immune system, which is the last line of defense. However, the immune system may not always be effective, and other non-immunological defenses might be favored to reduce the cost of parasite infection. Here we report that larvae of the moth Lobesia botrana can rapidly accelerate their development and reach maturity earlier in response to cues perceived at a distance from parasitoids. Such a phenotypically plastic life history shift, induced by the perception of deadly enemies in the environment, is likely to be an adaptive defensive strategy to prevent parasitoid attack, and has important implications in host-parasite dynamics. - Funding: Funding was provided by the CNRS and the ANR (ANR07-JCJC-0134 and ANR08-JCJC-0006 and the Conseil Regional de Bourgogne. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Parasites are omnipresent and can dramatically impact host growth, survival and reproduction, which together determine host life history [1,2]. When threatened by parasite infection, the host can reduce its loss of fitness by using its immune system to control the parasite. However, the immune system of the host is not always effective, and as an alternative it can reduce adverse parasite effects by facultative adjustment of its life history parameters [3,4,5]. For example, freshwater snails and crustaceans infected by castrating parasites reach reproductive maturity earlier [3,5], ensuring production of some offspring before the effects of castration establish. Such parasite-induced life history transitions often result in the reallocation of resources from growth to reproduction [6]. Consequently, hosts that mature earlier are smaller, which is often correlated with low fecundity and reduced longevity [1,2]. The animal kingdom includes numerous vertebrate [7] and invertebrate [8] correlations examples of pre-reproductive life span with adult size and fecundity. Thus, as accelerated development imposes significant costs, the host should trigger life history transitions only when highly reliable cues indicate an imminent and severe parasitic infection. Parasite cues inducing life history transitions are often associated with the infection event [3,5] or stimulation of the host immune system [9,10]. However, hosts can benefit from shifting their life histories prior to infection, as this reduces the overall cost of infection. This requires that host can highly reliably sense cues predicting infection prior to its occurrence. For instance, life history changes were induced in freshwater snails by exposing them to water that contained a parasite, in the absence of infection [6]. For holometabolous herbivorous insects total enemy-induced mortality is higher during late developmental stages, and larval parasitoids kill more herbivores than do either predators or pathogens [11]. Therefore, parasitoids represent a major selective force shaping defensive strategies during larval stages of these insects. As the evolution of immune resistance to parasitoid attack has substantial constitutive costs [12], plastic shortening of the prereproductive life stages (i.e. reaching metamorphosis earlier) in response to cues indicating imminent larval parasitoid attack is likely to be favored among insect hosts. However, because early maturation is costly, representing a decrease in reproductive output, insect larvae are expected to have evolved highly accurate recognition of cues specific to parasitoids. In this study we assessed this hypothesis using the moth Lobesia botrana (a major grapevine pest) as a holometabolous herbivorous insect model system. Natural populations of L. botrana are the targets of numerous species of parasitoids [13]. These populations face variable temporal and spatial changes in parasitoid pressure, which determine temporally and spatially variable risks of attacks [14]. Here, we mimicked imminent parasitoid attacks by exposing larvae of L. botrana to the presence of parasitoid and non-parasitoid insects without physical contact, and monitored the time for these larvae to reach metamorphosis. If L. botrana larvae could sense cues indicating the presence of parasitoid, we expect they will shorten their larval development and reach m (...truncated)


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Fanny Vogelweith, Yannick Moret, Denis Thiery, Jérôme Moreau. Lobesia botrana Larvae Develop Faster in the Presence of Parasitoids, PLOS ONE, 2013, Volume 8, Issue 8, DOI: 10.1371/journal.pone.0072568