The Limits of Evolutionary Convergence in Sympatry: Reproductive Interference and Historical Constraints Leading to Local Diversity in Warning Traits

Abstract

Mutualistic interactions between defended species represent a striking case of evolutionary convergence in sympatry, driven by the increased protection against predators brought by mimicry in warning traits. However, such convergence is often limited: sympatric defended species frequently display different or imperfectly similar warning traits. The phylogenetic distance between sympatric species may indeed prevent evolution towards the exact same signal. Moreover, warning traits are also involved in mate recognition, so that trait convergence might result in heterospecific courtship and mating. Here, we develop a mathematical model to investigate the strength and direction of evolution of warning trait in defended species with different ancestral traits. Specifically, we determine the effect of phenotypic distances between ancestral trait states of sympatric defended species and of costs of heterospecific sexual interactions on imperfect mimicry and trait divergence. Our analytical results confirm that reproductive interference and historical constraints limit the convergence of warning traits, leading to either complete divergence, or imperfect mimicry. Our model reveals that imperfect mimicry evolves only when ancestral trait values differ between species due to historical constraints and highlights the importance of female and predator discriminations in the evolution of such imperfect mimicry. Our study thus provides new predictions on how reproductive interference interacts with historical constraints and may promote the emergence of novel warning traits, enhancing mimetic diversity.

Reproductive interference is stronger than expected in Heliconius butterflies

“…Our experiments demonstrated the inefficacy or nonexistence of cryptic color differences as behavioral reproductive barriers between co‐mimics for males of three Heliconius species, including an inter‐generic pair where such cryptic signal was expected. This discovery supports the hypothesis of reproductive interference representing a trade‐off related to the evolution of mimicry (Hausmann et al, 2023; Maisonneuve et al, 2023) and, consequently, as a potential cost of coexistence between co‐mimic species. This cost would be paid in the form of wasting time and energy resulting from males harassment, which would finally mean less time and energy spent on location and courting conspecific mates, on oviposition (Hausmann et al, 2023), on foraging and on resting, in addition to a greater exposition to potential predators.…”