Warning coloration, body size and the evolution of gregarious behavior in butterfly larvae

Abstract

Many species gain anti-predator benefits by combining gregarious behavior with warning coloration, yet there is debate over which trait evolves first, and which is the secondary adaptive enhancement. Body size can also influence how predators receive aposematic signals, and potentially constrain the evolution of gregarious behavior. To our knowledge, the causative links between the evolution of gregariousness, aposematism and larger body sizes have not been fully resolved. Here, using the most recently resolved butterfly phylogeny and an extensive new dataset of larval traits, we reveal the evolutionary interactions between important traits linked to larval gregariousness. We show that larval gregariousness has arisen many times across the butterflies, and aposematism is a likely prerequisite for gregariousness to evolve. We also find that body size may be an important factor for determining the coloration of solitary, but not gregarious larvae. Additionally, by exposing artificial 'larvae' to wild avian predation, we show that undefended, cryptic 'larvae' are heavily predated when aggregated but benefit from solitariness, whereas the reverse is true for aposematic prey. Our data reinforce the importance of aposematism for gregarious larval survival, whilst identifying new questions about the roles of body size and toxicity in the evolution of grouping behavior.

Towards an integrative approach to understanding collective behaviour in caterpillars

“…[ 15 ], shows only major sub-clades for five families analysed in McLellan et al . [ 12 ], with Lycaenidae excluded owing to their frequent, derived, larval associations with ant nests. The middle panel illustrates the proportion of gregarious (orange segment of the pie chart) and solitary genera (grey segment), and the number of independent transitions to gregariousness estimated by McLellan et al .…”

“…( b ) Established evolutionary links between traits demonstrate the restricted extent of our understanding of ecological interactions surrounding group living. The figure illustrates the results of a phylogenetic pathway analyses attempting to reconstruct causative transitions between multiple traits [ 12 ] across butterfly larvae. Arrows indicate putatively causative interactions, with positive effects in green and negative effects in red.…”

“…However, competition for resources between grouped individuals may impose a trade-off between body size and group size, as females are limited in the resources that they can allocate to each egg to ensure larger larvae [ 17 ]. A recent comparative study across butterflies found no evidence supporting a direct evolutionary interaction between final instar size and grouping, instead suggesting that body size probably increases before the evolution of collective behaviour, mediated by the acquisition of a warning signal as crypsis becomes less effective with increased size [ 12 ].…”

“…These two factors could, in theory, interact to alter group size, as dispersing individuals could form splinter groups when attraction remains high. Regardless, while late instar gregariousness is probably a derived behaviour [ 12 , 13 , 19 ], less is known about the evolution of ontogenetic behavioural switches in collective behaviour.…”

“…These sources of variation can provide the basis for understanding the evolution and adaptive benefits of social behaviour (e.g. [ 12 ]).…”