Complex modular architecture around a simple toolkit of wing pattern genes

Abstract

Identifying the genomic changes that control morphological variation and understanding how they generate diversity is a major goal of evolutionary biology. In Heliconius butterflies, a small number of genes control the development of diverse wing color patterns. Here, we used full genome sequencing of individuals across the Heliconius erato radiation and closely related species to characterize genomic variation associated with wing pattern diversity. We show that variation around color pattern genes is highly modular, with narrow genomic intervals associated with specific differences in color and pattern. This modular architecture explains the diversity of color patterns and provides a flexible mechanism for rapid morphological diversification.

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

“…The same is true for WntA in a recent hybrid zone study (Fig. 4.3b), where three noncoding regions were each associated to pattern variation in distinct subareas of the butterfly wing, with their combination constituting the complete phenotype (Van Belleghem et al 2017). Finally, the wg study reveals the modular evolution of three tissuespecific enhancers that collectively explain the pigmentation features of D. guttifera Koshikawa 2015).…”

“…As it turns out, replicated mapping within the H. erato and H. cydno radiations has identified six and four noncoding WntA alleles underlying ten distinct wing color shapes in these two species groups, respectively (Martin et al 2012;Papa et al 2013;Gallant et al 2014). WntA thus exemplifies how repeated cis-regulatory modification of a ligand gene can replicate both within and between species, spanning a phylogenetic spectrum ranging from recently evolved populations (Van Belleghem et al 2017) to distant lineages (Gallant et al 2014). Importantly, this multiallelism probably acts as a prerequisite for the formation of complex alleles, as it is likely that adjacent regulatory regions evolve by recombination between blocks that exist as standing variation, rather than solely by cumulative de novo mutations on the same DNA molecule (Rebeiz et al 2011;Martin and Orgogozo 2013).…”

“…Association mapping reveals at least three adjacent haplotype regions with distinct patterning effects in H. erato (Fig. 4.3b) and a single 1.8 kb indel perfectly associated to a polymorphic variant in a sympatric H. cydno alithea population (Gallant et al 2014;Van Belleghem et al 2017). This said, the ⁄ ä functional dissection of these genetic elements is reaching a technical limitation at this moment due to the inability to test for the function of each cis-regulatory region in butterflies, and we must gain insight into the evolution of ligand gene expression in analog models to explore the logic of cis-regulatory control.…”

Beyond mean allelic effects: A locus at the major color geneMC1Rassociates also with differing levels of phenotypic and genetic (co)variance for coloration in barn owls

“…In such a scenario, we would expect these putative sites to be less polymorphic when co-occurring with the rufous allele to explain the lower variance associated with this allele. The existence of other loci affecting coloration in the vicinity of the MC1R gene still needs to be assessed in the barn owl, but studies supporting modularization of genetic variation responsible for phenotypic variation render this possible (Van Belleghem et al 2016). This might have reduced genetic variation in the vicinity of the MC1R rufous allele owing to the hitchhiking effect of selection on the rufous allele, which has been observed in the MC1R of two populations of lizard species that evolved blanched colorations to adapt to the light soil of the White Sands ecosystem of New Mexico (Laurent et al 2016).…”

Supergene evolution triggered by the introgression of a chromosomal inversion

“…1a), each one matching to near perfection the colours and shapes of other toxic Lepidoptera (Heliconiinae, Danainae, Pericopiinae) 2 . This balanced polymorphism is controlled by a supergene locus (P) associated with an inversion polymorphism 2 that captures multiple genetic loci controlling wingpattern variation in butterflies and moths 12,[18][19][20][21] and allows multiple wing elements to be inherited as a single Mendelian character. The ancestral chromosomal arrangement, called Hn0, is associated with the recessive supergene allele 17 which controls the widely distributed morph silvana.…”