Convergence in sympatric swallowtail butterflies reveals ecological interactions as a key driver of worldwide trait diversification.

Ecological interactions can promote phenotypic diversification in sympatric species. While competition can enhance trait divergence, other ecological interactions may promote convergence in sympatric species. Within butterflies, evolutionary convergences in wing color patterns have been reported between distantly related species, especially in females of palatable species, where mimetic color patterns are promoted by predator communities shared with defended species living in sympatry. Wing color patterns are also often involved in species recognition in butterflies, and divergence in this trait has been reported in closely related species living in sympatry as a result of reproductive character displacement. Here, we investigate the effect of sympatry between species on the convergence vs. divergence of their wing color patterns in relation to phylogenetic distance, focusing on the iconic swallowtail butterflies (family Papilionidae). We developed an unsupervised machine learning-based method to estimate phenotypic distances among wing color patterns of 337 species, enabling us to finely quantify morphological diversity at the global scale among species and allowing us to compute pairwise phenotypic distances between sympatric and allopatric species pairs. We found phenotypic convergence in sympatry, stronger among distantly related species, while divergence was weaker and restricted to closely related males. The convergence was stronger among females than males, suggesting that differential selective pressures acting on the two sexes drove sexual dimorphism. Our results highlight the significant effect of ecological interactions driven by predation pressures on trait diversification in Papilionidae and provide evidence for the interaction between phylogenetic proximity and ecological interactions in sympatry, acting on macroevolutionary patterns of phenotypic diversification.

Convergence in sympatry: Evolution of blue-banded wing pattern in Morpho butterflies.

Species interactions such as mimicry can promote trait convergence but disentangling this effect from those of shared ecology, evolutionary history, and niche conservatism is often challenging. Here by focusing on wing colour pattern variation within and between three butterfly species living in sympatry in a large proportion of their range, we tested the effect of species interactions on trait diversification. These butterflies display a conspicuous iridescent blue coloration on the dorsal side of their wings and a cryptic brownish colour on the ventral side. Combined with an erratic and fast flight, these colour patterns increase the difficulty of capture by predators and contribute to the high escape abilities of these butterflies. We hypothesize that, beyond their direct contribution to predator escape, these wing patterns can be used as signals of escape abilities by predators, resulting in positive frequency-dependent selection favouring convergence in wing pattern in sympatry. To test this hypothesis, we quantified dorsal wing pattern variations of 723 butterflies from the three species sampled throughout their distribution, including sympatric and allopatric situations and compared the phenotypic distances between species, sex and localities. We detected a significant effect of localities on colour pattern, and higher inter-specific resemblance in sympatry as compared to allopatry, consistent with the hypothesis of local convergence of wing patterns. Our results provide support to the existence of escape mimicry in the wild and stress the importance of estimating trait variation within species to understand trait variation between species, and to a larger extent, trait diversification at the macro-evolutionary scale.