Towards an integrative approach to understanding collective behaviour in caterpillars

Abstract

To evolve, and remain adaptive, collective behaviours must have a positive impact on overall individual fitness. However, these adaptive benefits may not be immediately apparent owing to an array of interactions with other ecological traits, which can depend on a lineage's evolutionary past and the mechanisms controlling group behaviour. A coherent understanding of how these behaviours evolve, are exhibited, and are coordinated across individuals, therefore requires an integrative approach spanning traditional disciplines in behavioural biology. Here, we argue that lepidopteran larvae are well placed to serve as study systems for investigating the integrative biology of collective behaviour. Lepidopteran larvae display a striking diversity in social behaviour, which illustrates critical interactions between ecological, morphological and behavioural traits. While previous, often classic, work has provided an understanding of how and why collective behaviours evolve in Lepidoptera, much less is known about the developmental and mechanistic basis of these traits. Recent advances in the quantification of behaviour, and the availability of genomic resources and manipulative tools, allied with the exploitation of the behavioural diversity of tractable lepidopteran clades, will change this. In doing so, we will be able to address previously intractable questions that can reveal the interplay between levels of biological variation. This article is part of a discussion meeting issue ‘Collective behaviour through time’.

A multi-scale review of the dynamics of collective behaviour: from rapid responses to ontogeny and evolution

“…[ 162 ] make the argument that lekking, which occurs when multiple males congregate to perform mating displays, might be best viewed through the lens of collective behaviour, whereby the emergent properties of the lek can be understood as the result of small, local-scale individual-level interactions. Also, while much of collective behaviour research has focused on fishes, birds and eusocial insects, McLellan & Montgomery [ 163 ] highlight how caterpillars (i.e. Lepidopteran larvae) exhibit many of the same characteristics we value in these other animal taxa and may be especially tractable systems for investigating the development and mechanistic underpinnings of collective behaviours.…”

Selfish herd effects in aggregated caterpillars and their interaction with warning signals

“…One example comes from laboratory experiments conducted by McClure and Despland [6], who found that Drepana arcuata caterpillars exposed to predation by spiders, stinkbugs, and parasitoid wasps sustained fewer attacks when positioned near the centre of their aggregation compared to those on the periphery. However, while McClure and Despland's findings suggest that group position has an effect on larval survival against invertebrate predators, testing this was not their focus, and questions remain around how other relevant predators, such as birds, might preferentially attack aggregated individuals [18]. To date, only one experiment has formally tested how avian predation risk is associated with lepidopteran larval DOD, revealing that, as 4 hypothesised, predation risk decreases with DOD for cryptic prey in static representations of processionary columns [19].…”

Collective synchrony of mating signals modulated by ecological cues and social signals in bioluminescent sea fireflies

“…Just across arthropods, synchronised behaviours are taxonomically scattered and probably arose multiple times from within groups without synchronous displays, suggesting convergent evolutionary events [18,19]. Outside the defensive visual displays of lepidopteran caterpillars [20] and vibrations of treehoppers [21], synchronised mating signals are known from choruses of singing orthopterans [22,23] and cicadas [8], the waving claws of fiddler crabs [24,25], and most famously, the glowing, flash bursts of synchronous fireflies found in Southeast Asia and the Americas [26,27]. These fireflies differ from their non-synchronous relatives, and as in other collective behaviours, seem to use local rules such as responding to the timing [28,29] of visual neighbours [27], which produces emergent synchrony.…”