Perfect mimicry between Heliconius butterflies is constrained by genetics and development

Abstract

Müllerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. The butterfly species Heliconius erato and Heliconius melpomene have a large diversity of co-mimicking geographic races with remarkable resemblance in melanic patterning across the midforewing that has been linked to expression patterns of the gene WntA. Recent CRISPR/Cas9 experiments have informed us on the exact areas of the wings in which WntA affects color pattern formation in both H. erato and H. melpomene, thus providing a unique comparative dataset to explore the functioning of a gene and its potential effect on phenotypic evolution. We therefore quantified wing color pattern differences in the mid-forewing region of 14 co-mimetic races of H. erato and H. melpomene and measured the extent to which mimicking races are not perfectly identical. While the relative size of the mid-forewing pattern is generally nearly identical, our results highlight the areas of the wing that prevent these species from achieving perfect mimicry and demonstrate that this mismatch can be largely explained by constraints imposed by divergence in the gene regulatory network that define wing color patterning. Divergence in the developmental architecture of a trait can thus constrain morphological evolution even between relatively closely related species.

Conspicuousness, phylogenetic structure, and origins of Müllerian mimicry in 4000 lycid beetles from all zoogeographic regions

“…We assume that there are several potential predictors of the diversity of aposematic signalling in a region: phylogenetic diversity, alpha-diversity, and abundance. Further factors include the ecosystem diversity 62 , 124 , 125 and genetic constraints 126 on which we do not have sufficient information. The evaluation of considered factors depends on the availability of data.…”

Capturing and analyzing pattern diversity: an example using the melanistic spotted patterns of leopard geckos

“…Similarly, in horses, two genes with different alleles determine the occurrence and amount of melanistic spots on a white colored coat ( Druml et al, 2017 ). The availability of the leopard gecko genome ( Xiong et al, 2016 ), the relative easiness to breed this species, and the existence of CRISPR-Cas9 technology already tested to create mutations in lizards ( Rasys et al, 2019 ) will allow us to develop future research to uncover the genetic basis of variation in pattern elements in this species, similarly to what has been done for mammals and other non-mammalian model species ( Van Belleghem et al, 2020 ; Concha et al, 2019 ).…”

Reinventing the wheel? Reassessing the roles of gene flow, sorting and convergence in repeated evolution

“…Molecular convergence is typically considered to be a slow process, as it requires independent mutations to evolve and spread through distinct populations (see Barton & Keightley, 2002; Pujol et al, 2018). Increasingly, however, molecular studies are revealing cases of convergence in which very similar phenotypes have evolved recently among closely related lineages via independent genetic mutations (e.g., Concha et al, 2019; Urban et al, 2021; Van Belleghem et al, 2020). In sister populations of freshwater fishes, for instance, independent losses of marine migration have apparently been achieved via different pathways, leading to different levels of salinity tolerance in different landlocked populations (Delgado et al, 2019, 2020).…”