Abstract

Aggregation can confer advantages in animal foraging, defense, and thermoregulation. There is a tight connection between the evolution of insect sociality and a highly effective immune system, presumably to inhibit rapid disease spread in a crowded environment. This connection is less evident for animals that spend only part of their life cycle in a social environment, such as noneusocial gregarious insects. Our aim was to elucidate the effects of group living by the gregarious larvae of the Glanville fritillary butterfly with respect to individual performance, immunity, and susceptibility to a parasitoid. We were also interested in the role of family relative to common postdiapause environment in shaping life‐history traits. Larvae were reared at high or low density and then exposed to the pupal parasitoid wasp Pteromalus apum, either in presence or absence of a previous immune challenge that was used to measure the encapsulation immune response. Surviving adult butterflies were further tested for immunity. The wasp offspring from successfully parasitized butterfly pupae were counted and their brood sex ratios assessed. Larvae reared at high density grew larger and faster than those at low density. Despite high mortality due to parasitism, survival was greater among individuals with high pupal immunity in both density treatments. Moreover, butterfly pupae reared at high density were able to kill a larger fraction of individuals in the parasitoid broods, although this did not increase survival of the host. Finally, a larger proportion of variation observed in most of the traits was explained by butterfly family than by common postdiapause rearing environment, except for adult survival and immunity, for which this pattern was reversed. This gregarious butterfly clearly benefits from high conspecific density in terms of developmental performance and its ability to fight a parasitoid. These positive effects may be driven by cooperative interactions during feeding.

Highlights

  • Some phase-­polyphenic insects have evolved a plastic response to anticipate the increased infection risk due to crowding, which consists of upregulating their immunity when in the gregarious phase. These examples suggest that the infection risk caused by recurrent crowding has presumably led to the evolution of a plastic immune system, similar to that of eusocial insects, but less structured. These findings suggest that the regulation of the immune system of species with intermediate life histories should share some characteristics with both social and solitary species

  • We found that M. cinxia larvae developed faster and reached a larger pupal mass when reared at high density, suggesting a positive effect of crowding

  • High-­density individuals showed a greater immune attempt by killing a larger fraction of parasitoids per brood than did those reared in low density

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Summary

Introduction

Several potential advantages of this behavior have been found, ranging from predator avoidance to foraging and dispersal efficiency, thermoregulation, or a combination of these (see Krause & Ruxton, 2002 for details). Aggregation can be costly, as a group can be detected by predators and infections spread rapidly in a crowded environment (Arneberg, Skorping, Grenfell, & Read, 1998). Resource competition among group members may occur (Parrish & Edelstein-­Keshet, 1999). Group aggregation occurs only during particular activities or life cycle stages. Some animals forage in herds, and birds migrate in flocks (Parrish & Edelstein-­Keshet, 1999)

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