Social evolution in the Lepidoptera: ecological context and communication in larval societies

Abstract

We review key ecological and behavioral mechanisms under lying the origin and maintenance of larval sociality in the Lepidoptera. Using communication contexts of group defense, cohesion and recruitment as a framework we relate social complexity among gregarious caterpilla~ to three panerns of foraging: patch-restricted, nomadic, and central-place. A review ofthe incidence oflarval gregarious ness in the Lepidoptera demonstrates that sociality is wid"e spread in the order, occurring in twenty or more families representing thirteen ditrysian superfamilies, and it is likely to have evolved numerous times in response to differ ent selective pressures. We specifically address the role of sociality in larval defense and resource use, with a focus on (I) signal enhancement in communication systems, (2) differential larval vulnerability, and (3) ant association. Larval Lepidoptera experience the greatest likelihood of mortality in the earliest instars; larval sociality enhances defensive and resource-exploitation signals in these in stars, positively influencing survivorship and larval growth. Disease, predation and parasitism, nutrition, and inclusive fitness are discussed in terms ofcosts and benefits ofgroup living. Finally, we identify two areas where additional research will con tribute significantly to an understanding ofsocial evolution in the Lepidoptera: (I) comparative phy logenetic studies, using ecological and communicative characters to trace the origins of caterpillar societies and transitions among them, and (2) larval behavior and ecol ogy, focusing on kin discrimination abilities, assessment of colony genetic strucrure, and most importantly on the means and contexts of caterpillar communication.

Vibrational Communication and the Ecology of Group-Living, Herbivorous Insects

“…This process also occurs in the chemical signals produced during recruitment communication in some eusocial insects and in tent caterpillars (Costa and Pierce, 1997;Hölldobler and Wilson, 1990). This coordination of signaling may provide a means by which individuals with a common interest can enhance the signals of other colony or group members (see Costa and Pierce, 1997).…”

“…Other benefits of grouping can include increased water uptake (Lockwood and Story, 1986), slower water loss (Friedlander, 1965), and enhanced thermoregulation (Seymour, 1974). Indeed, Costa and Pierce (1997) suggest that there may often be sufficient direct benefits of group living that grouping is favored whether or not the individuals are genetically related. One line of evidence supporting this view is that, in many species, groups that encounter each other merge into a larger group composed of individuals from different family groups, species, or genera (Carne, 1962;Wood, 1984Wood, , 1993.…”

“…1C; deVries, 1990;Travassos and Pierce, 2000). The signals of larval and pupal lycaenids appear to function in attracting and maintaining an association with ants (deVries, 1991;Travassos and Pierce, 2000).…”

Host marking behavior in phytophagous insects and parasitoids

“…The evolution of host-marking under kin selection may require restrictive conditions such as limited dispersal among related conspecifics (Godfray, 1993). Such restrictions notwithstanding, kin selection may account at least in part for the evolution of trail marking among social caterpillars (Costa & Pierce, 1997) or the repellent scent marks placed on recently exploited flowers by honey bees and bumblebees (Goulson et al, 1998).…”

Diversification of gut morphology in caterpillars is associated with defensive behavior

“…A lack of well-resolved phylogenies at many lower taxonomic levels among the Lepidoptera prevents phylogenetically controlled comparative analyses (Costa and Pierce, 1998). However, after applying the Runs Test as implemented in Phylogenetic Independence 2.0 software (Reeve and Abouheif, 2003), regurgitation behavior was not found to be phylogenetically autocorrelated (1000 iterations, Cstat=17.48, P=0.004).…”