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.

Patterns of morphological variation highlight the effect of natural selection on eyespots modularity in the butterfly Morpho telemachus.

Morphological correlations can not only stem from developmental constraints but also from selective pressures. Butterfly eyespots are repeated wing color pattern elements, widespread across species. As developmental serial homologs, they are controlled by similar developmental pathways imposing correlations among eyespots: selection on a single eyespot may induce correlated responses in all eyespots. We study the variations in the ventral eyespots of Morpho telemachus, where two different selective regimes are likely to act: while most eyespots are always-visible, two eyespots are conditionally displayed: hidden at rest, they can be exposed when the butterflies are threatened, or during sexual interactions. We investigate how such contrasted selection across eyespots can alter the covariations imposed by their shared developmental origin. We quantified eyespots covariations within a large population of M. telemachus and compared the observed patterns to those found in M. helenor, where all eyespots are always-visible and thus probably affected by a similar selection regime. We found that M. telemachus conditionally displayed eyespots are less variable than always-visible eyespots and that these two eyespots form a separate variational module in this species, in contrast to M. helenor. Our results suggest that eyespots covariations were shaped by selection, highlighting how natural selection may promote the evolution of modularity.

Evidence of attack deflection suggests adaptive evolution of wing tails in butterflies.

Predation is a powerful selective force shaping many behavioural and morphological traits in prey species. The deflection of predator attacks from vital parts of the prey usually involves the coordinated evolution of prey body shape and colour. Here, we test the deflection effect of hindwing (HW) tails in the swallowtail butterfly Iphiclides podalirius. In this species, HWs display long tails associated with a conspicuous colour pattern. By surveying the wings within a wild population of I. podalirius, we observed that wing damage was much more frequent on the tails. We then used a standardized behavioural assay employing dummy butterflies with real I. podalirius wings to study the location of attacks by great tits Parus major. Wing tails and conspicuous coloration of the HWs were struck more often than the rest of the body by birds. Finally, we characterized the mechanical properties of fresh wings and found that the tail vein was more fragile than the others, suggesting facilitated escape ability of butterflies attacked at this location. Our results clearly support the deflective effect of HW tails and suggest that predation is an important selective driver of the evolution of wing tails and colour pattern in butterflies.