Pervasive convergence in flight patterns enhances mimicry in aposematic butterflies

Authors: QUESTE, LUCIE - University Of York; PAGE, EDWARD - University Of York; ROSSER, NEIL - Harvard University; MALLET, JAMES - Harvard University; Srygley, Robert; MCMILLAN, W OWEN - Smithsonian Tropical Research; DASMAHAPATRA, KANCHON - University Of York

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/10/2024
Publication Date: 2/26/2024
Citation: Queste, L.M., Page, E., Rosser, N., Mallet, J.K., Srygley, R.B., McMillan, W., Dasmahapatra, K.K. 2024. Pervasive convergence in flight patterns enhances mimicry in aposematic butterflies. Proceedings of the National Academy of Sciences (PNAS). 121(11). Article e230088612. https://doi.org/10.1073/pnas.2300886121.
DOI: https://doi.org/10.1073/pnas.2300886121

Interpretive Summary: Flight is a complex trait, integrating behavior, physiology, ecology and evolution. In rare cases, mimicry among distasteful butterfly species, also known as Mullerian mimicry, and mimicry between palatable and distasteful species, or Batesian mimicry, have been shown to influence flight pattern. Using video footage of mimetic Heliconius butterflies, we quantified the flight pattern of 35 species and found that butterflies belonging to the same colour pattern mimicry group have also converged evolutionarily in flight behavior. Behavioral mimicry also extends to the distantly-related Ithomiini tribe. For the first time, we demonstrate the presence of behavioral mimicry across a large, phylogenetically diverse group, and show that complex mimicry that includes both wing color pattern and flight behavior has evolved between species across a broad range of evolutionary timescales.

Technical Abstract: The evolution of flight was a key innovation in the adaptive radiation of insects. However, it is difficult to disentangle the selective pressures affecting this complex trait. We investigate the evolutionary drivers of flight patterns in neotropical heliconiine butterflies, well-known for the widespread mimicry of their aposematic wing color patterns. We quantify the flight patterns (wing beat frequency and wing angles) of 289 butterflies representing 32 heliconiine and 3 ithomiine species. After controlling for shared ancestry, we show that species cluster by mimicry group for both flight metrics, and mimetic convergence explains up to 66% of the variation in flight pattern within the tribe. The flight characteristics of the silvaniform mimicry group are particularly divergent, apparently due to convergence with distantly-related ithomiine species. Locomotor mimicry also extended to explaining intraspecific variation in flight, indicating that this convergence can occur over relatively short evolutionary timescales. Our results also suggest that this flight convergence is driven by aposematic signaling rather than shared habitat between co-mimics. To our knowledge, this is the first study demonstrating that behavioral mimicry can occur over a wide range of evolutionary timescales from 2 to 70 million years.