Hiding among holes: mechanisms underlying the evolution of masquerade in flea beetles (Chrysomelidae)

Authors: FOLGAR-CAMEAN, YERAY - Universidad De Santiago De Compostela; GOMEZ-RODRIGUEZ, CAROLA - Universidad De Santiago De Compostela; Konstantinov, Alexander - Alex; BASELGA, A. - Universidad De Santiago De Compostela

Submitted to: Journal of Animal Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/23/2021
Publication Date: 10/9/2021
Citation: Folgar-Camean, Y., Gomez-Rodriguez, C., Konstantinov, A.S., Baselga, A. 2021. Hiding among holes: mechanisms underlying the evolution of masquerade in flea beetles (Chrysomelidae). Journal of Animal Ecology. 47(2):137-145. https://doi.org/10.1111/een.13096.
DOI: https://doi.org/10.1111/een.13096

Interpretive Summary: Leaf beetles, especially flea beetles, are among the most important insects for U.S. agriculture. Many are serious pests and feed on crops destroying valuable plants costing millions of dollars annually. Others are important biological control agents that can be used to control unwanted and invasive weeds. This work describes possible mechanisms that drive evolution of a masquerade mimicry in flea beetles. Masquerading flea beetles, while feeding, make holes in leaf surfaces of their host plants, which approximate beetle bodies in size and color, which helps beetles to avoid predators. This study will be useful to biological control workers, taxonomists, ecologists, and anyone interested in plant feeding beetles and their interaction with host plants.

Technical Abstract: Camouflage can be associated with different evolutionary pressures affecting phytophagous insects on their host plants. The small herbivorous flea beetles (Chrysomelidae: Alticini) evolved a masquerading strategy by hiding among their own feeding damage. Colour and size similarities between beetle bodies and their feeding damage of the leaf surfaces on which they live, may act as a defence that reduces predation by visually oriented predators. Here we analyse the evolutionary origin of this feature using an example of the flea beetle fauna of France. It is one of the best known in the world containing 284 species with one of the best known host plants. We aim to assess whether the type of leaf tissues have selected the colour and size of beetle species because of its propensity to being damaged in a particular way (H1) or, alternatively, if morphological characteristics of the beetle have selected the damage pattern it produces (H2). We built two bipartite networks of feeding interactions between beetle species and their host plants (families and genera, separately). We first estimated network modules and then evaluated if the beetles within each module shared a common characteristic, colour tone or size, by comparing colour and size distributions within modules with null expectations. Feeding interactions among host plants were non-randomly distributed and highly modular. Around one third and one fourth of the modules showed significant differences in tone and size distribution, respectively, with null models. The study shows that the evolutive origin of the flea beetle masquerade can be partially explained by both hypotheses considered here. Some host plants seem to restrict feeding damage appearance on their leaves, favouring the survival of specific beetles with matching colour and size (H1). However, in most plant taxa the random distribution of beetle colour and size suggests the existence of beetle-associated constraints that exert a selective pressure for the coleopteran to do a particular leaf damage with similar colour and size to its own body (H2). In conclusion, we found partial support for both types of restrictions associated with plants (H1) and beetles (H2), which together would have contributed to the appearance of masquerade among alticines.