Influence of temperature and parasitism by
Asobara tabida on larval pupation behaviour in
two Drosophila species
Josso C.
1, Moiroux J.
2, Vernon P.
2, van Baaren J.
2, van Alphen J.J.M
2Author affiliations 1 UMR INRA Biologie des Populations appliquée à
la Protection des Plantes
Bât 25 – Campus de Beaulieu – 263 Avenue du Général Leclerc – 35042 RENNES
celine.josso@univ-rennes1.fr 2
UMR CNRS ECOBIO – Bât 14 – Campus de Beaulieu – 263 Avenue du Général Leclerc – 35042 RENNES
Article Informations Submitted to Naturwissenschaften
Key words temperature, adaptive behavior, Drosophila,
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Abstract
In insects, pupation site selection behavior has large consequences for survival. Here we investigate the combined effect of temperature and parasitism by the parasitoid Asobara tabida on larval pupation behavior in two of its main Drosophila sp. hosts differing in their climate origin. We found that larvae of Drosophila melanogaster - from (sub) tropical regions - placed at 25°C pupate higher in rearing jars, i.e where conditions are drier, than those placed at 15°C. The opposite pattern was observed for D. subobscura larvae - from temperate regions - which pupate lower, i.e on or near the substrate in relatively moist conditions, than those placed at 15°C. When placed at 25°C, parasitized larvae of the two species pupated more closely to the substrate than unparasitized ones. Moreover, Drosophila larvae that had been exposed to A. tabida but were not parasitized pupated lower than control unparasitized larvae. Both stung larvae and parasitized larvae differed from control ones in their pupation behavior. These results provide new insights into previous findings of host behavior manipulation by A. tabida larvae.
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INTRODUCTION
The abiotic and biotic conditions experienced by organisms influence their geographical and habitat distribution directly (e.g. Gaston 2003, 2009; Schnebel and Grossfield 1992). Temperature and parasitism are examples of such environmental conditions and both have major effects on life-history traits of organisms. Temperature affects life history via physiology, ecology and so influences fitness of ectotherms (Dillon et al. 2009). Extreme temperatures are injurious and potentially lethal, but even temperature within those lethal limits impacts performance and ultimately individual fitness (Dillon et al. 2009). Parasitoids are common natural enemies of many insect species. As their successful attacks kill the host, the latter is expected to be under strong selection to evolve means of defending itself (Kraaijeveld and Godfray 2003). Parasitoids display a large variety of mechanisms permitting them to manipulate their hosts’ behavior and/or physiology to the benefit of their own development (for review, see Beckage and Gelman 2004).
Since insect pupae are immobile, they remain exposed to potentially harmful factors (desiccation, predation, hyperparasitism by pupal parasitoids, fungal infection, etc.) for varied periods of time. Pupation site selection during the late larval stage can thus be critical for survival (Schnebel and Grossfield 1992), and in this way, this trait is supposed to be under strong selection.
The pupation behavior of larvae has been well documented in Drosophila species. A number of environmental factors, studied independently for the greater part, including temperature (Schnebel and Grossfield 1992; Vandal and Shivanna 2007), light or darkness (Markow 1979), moisture (Sameoto and Miller 1968), density (Sameoto and Miller 1968; Joshi and Mueller 1993), the presence of predators or parasitism (Seyahooei et al. 2009) have been shown to influence the pupation behavior of Drosophila larvae. When tested independently, the effects of each parameter on larval pupation-height responses differ for each species studied. Schnebel and Grossfield (1986, 1992) have underlied the complexity of the relation between temperature and pupation height. The response of a species in pupation-height at one temperature extreme cannot be used to predict responses at the other temperature extreme, and temperature effects on pupation height in one species do not consistently reflect the effects on other species within the Drosophila group.
A recent study of Seyahooei et al. (2009) found that attack of larvae of the same host (Drosophila melanogaster) by five species of a parasitoid (Asobara sp.) affects host pupation height in different ways. The authors hypothesized that Asobara sp. are able to manipulate the
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behavior of D. melanogaster larvae to achieve their own optimal pupation strategy, because it is the host larva that choses the pupation site. In fact, parasitoids and hosts may often differ in optimal pupation strategies. This is especially true for parasitoids spending more time in the puparium than their host (as Asobara sp.), thus vulnerable to dangers for a longer time. Seyahooei et al. (2009) did not consider the influence of a particular parasitoid species on pupation height of different host species.
Drosophila larvae are under attack of several parasitoid species, of which the most common in Europe are the braconid Asobara tabida, and the figitids Leptopilina heterotoma and L. boulardi (Carton et al. 1986). Within Asobara tabida’s range, most of the potential host species belong to the obscura and the melanogaster group (Kraaijeveld and van der Wel 1994). While Drosophila larvae are pupating, Asobara tabida is still completing its development inside the host.
The pupation behavior of larvae has been well documented in species belonging to the melanogaster group (e.g. D. melanogaster, D. simulans, etc.) (Sameoto and Miller 1968; Schnebel and Grossfield 1992; Casares et al. 1997; Hodge and Caslaw 1998; Vandal et al. 2008; Seyahooei et al. 2009; Beltrami et al. 2010), but has been much less studied in species belonging to the obscura group (e.g. Drosophila subobscura, D. pseudoobscura, etc.) (Markow 1979; Gaso et al. 1988). Moreover, to our knowledge, the combined effect of several parameters on pupation height has never been documented.
The aim of the present work was to investigate the effects of temperature and parasitism as well as their interaction, on the pupation behavior of larvae, using a parasitoid, Asobara tabida, and its two main hosts, which differ in climate origin: in Northwestern Europe (i.e in temperate regions), Drosophila subobscura Collin is the most abundant host species, while in mediterranean regions, D. melanogaster Meigen is the main host (Mollema 1988)
We expected that i) temperature would affect the pupation site selection of the two Drosophila species differently, because of their different climate origin. At a higher temperature, the risks associated with desiccation should result in a decrease of D. subobscura pupation height and a selection of pupation sites near the substrate in relatively moist conditions. D. melanogaster is expected to be more resistant to desiccation, and its larvae should be less constrained in choosing pupation sites. Hence, we expect them to pupate further away from the substrate than D. subobscura larvae at the same temperature, ii) because of the differences in selection due to differences in the time spent within the puparium, the effect of temperature on pupation behavior differs between hosts and parasitoids. At higher temperature, parasitized hosts need to be protected from desiccation for
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a longer period of time and are, therefore, expected to pupate closer to the substrate than unparasitized ones. iii) If parasitoid larvae are able to manipulate host pupation behavior to their own advantage (Seyahooei et al. 2009), parasitized host larvae might choose a different pupation site than unparasitized larvae. We expect A. tabida to affect pupation site behavior of its two main hosts in the same way. iv) Finally, we compared pupation behavior of unparasitized larvae with unparasitized ones that had been exposed to the parasitoid, to study if such exposure changes pupation site choice.