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.
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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)