Adaptive evolution of butterfly wing shape: from morphology to behaviour

Abstract

Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho-functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro-and micro-evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro-evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness-related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex-specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co-evolution between morphology and flight behaviour.

Testing the role of ecological selection on colour pattern variation in the butterflyParnassius clodius

“…In another study using data from multiple butterfly families (Lycaenidae, Nymphalidae, Papilionidae, and Pieridae), Stelbrink et al () found that colour lightness increased (butterflies became less dark) with increasing solar radiation, corroborating the thermal melanism hypothesis. We note that these conclusions are based on statistical associations, and require additional experiments, such as reciprocal transplants or biophysical modelling, to confirm fitness effects of the observed patterns of local adaptation (Le Roy, Debat, & Llaurens, ).…”

Altitude and life‐history shape the evolution ofHeliconiuswings

“…C). Aspect ratio was used as a proxy of wing shape, as it has been widely used in previous studies and correlates to gliding efficiency (Le Roy et al ). The data were checked for visual outliers on scatter‐plots, which were examined, and removed from the analyses if the wing extraction pipeline had failed.…”

“…; Le Roy et al. ). In butterflies, males tend to spend more time looking for mates and patrolling territories, while females focus their energy on searching for suitable host plants for oviposition (Rossato et al.…”

“…A recent review assessing the ecology of butterfly flight, identified habitat, predators, and sex‐specific behaviors as the selection forces most likely driving wing morphology variation, but highlighted the need for further phylogenetic comparative studies that identify the adaptive mechanisms shaping wings (Le Roy et al. ).…”

“…In butterflies, high aspect ratios, that is, long and narrow wings, reduce drag caused by wing tip vortices, thus lowering the energy required for flight and promoting gliding for longer distances (Le Roy et al. ). Variation in wing phenotypes can occur at the microhabitat level, for example, Morpho butterfly clades in the understory have rounder wings than canopy‐specialist clades, presumably for increased maneuverability (Chazot et al.…”