The limits of evolutionary convergence in sympatry: reproductive interference and historical constraints leading to local diversity in warning traits

Abstract

Mutualistic interaction between defended species is a striking case of evolutionary convergence in sympatry, driven by the increased protection against predators brought by mimicry. 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 implied in mate recognition, so that trait convergence might result in heterospecific courtship and mating. Here, we investigate the strength and direction of convergence in warning trait in defended species with different ancestral traits, using a mathematical model. We specifically determine the effect of phenotypic distances among ancestral traits of converging species, and costs of heterospecific sexual interactions on imperfect mimicry and trait divergence. Our analytical results confirm that reproductive interference limits the convergence of warning trait, leading to either imperfect mimicry or complete divergence. More surprisingly, our model pinpoints that reproductive interference can change the direction of convergence depending on the relative species densities. We also show that reproductive interference can generate imperfect mimicry only between species with different ancestral traits. Our model therefore highlights that convergence triggered by Müllerian mimicry not only depends on relative defence levels, but that relative species densities, heterospecific sexual interactions and ancestral traits interfere in the direction and strength of convergence between species.

Evolutionary origins of sexual dimorphism : Lessons from female-limited mimicry in butterflies.

“…Females deceived by the colour pattern then need to deploy substantial efforts to avoid the heterospecific mating. Theoretical studies highlight that RI promotes the evolution of females preference different from the phenotype of the other sympatric species because it reduces the number of costly sexual interactions [McPeek and Gavrilets, 2006, Yamaguchi and Iwasa, 2013, Maisonneuve et al, 2021]. These females preference, caused by RI may therefore explain the evolution of sexual dimorphism in mimetic species [Yamaguchi and Iwasa, 2013].…”

Evolutionary origins of sexual dimorphism: Lessons from female‐limited mimicry in butterflies

“…2020) that may impede divergence from the ancestral trait (Maisonneuve et al. 2021). Phylogenetic analyses show that FLM derived from sexually monomorphic non‐mimetic ancestors (Kunte 2009, Timmermans et al.…”

“…In line with this expectation, Su et al (2015) showed that in a mimetic butterflies where males and females mimic the same species, females are more prefect mimics than males, suggesting also that some constraints limits perfect mimicry in males. Wing pattern evolution is also shaped by developmental constraints (Van Belleghem et al 2020) that may impede divergence from the ancestral trait (Maisonneuve et al 2021). Phylogenetic analyses show that FLM derived from sexually monomorphic non-mimetic ancestors (Kunte 2009, Timmermans et al 2017 suggesting that mimicry in FLM species is associated with a costly displacement from an ancestral non-mimetic phenotype.…”

“…Theoretical studies highlight that the reproductive interference between sympatric species influence the evolution of traits used as mating cues. Reproductive interference indeed promotes the evolution of female preference toward traits differing from the phenotype displayed in other sympatric species, because it reduces the number of costly sexual interactions (McPeek & Gavrilets 2006, Maisonneuve et al 2021, Yamaguchi & Iwasa 2013. However these studies do not consider the independent evolution male and female traits.…”

“…In species exhibiting FLM, reproductive interference may thus inhibit natural selection in males, while females become mimetic. Theoretical studies show that reproductive interference can totally impair the evolution of mimicry (Boussens-Dumon & Llaurens 2021) or lead to imperfect mimicry (Maisonneuve et al 2021) therefore suggesting that reproductive interference might indeed be a relevant ecological interaction preventing mimicry in males. In the model investigating the effect of reproductive interference on mimicry described in Boussens-Dumon and Llaurens (2021), color-patten based assortative mating was assumed, preventing the study of the evolution of disassortative preferences in females.…”