Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

Abstract

The mimetic butterflies Heliconius erato and Heliconius melpomene have undergone parallel radiations to form a near-identical patchwork of over 20 different wing-pattern races across the Neotropics. Previous molecular phylogenetic work on these radiations has suggested that similar but geographically disjunct color patterns arose multiple times independently in each species. The neutral markers used in these studies, however, can move freely across color pattern boundaries, and therefore might not represent the history of the adaptive traits as accurately as markers linked to color pattern genes. To assess the evolutionary histories across different loci, we compared relationships among races within H. erato and within H. melpomene using a series of unlinked genes, genes linked to color pattern loci, and optix, a gene recently shown to control red colorpattern variation. We found that although unlinked genes partition populations by geographic region, optix had a different history, structuring lineages by red color patterns and supporting a single origin of red-rayed patterns within each species. Genes closely linked (80-250 kb) to optix exhibited only weak associations with color pattern. This study empirically demonstrates the necessity of examining phenotype-determining genomic regions to understand the history of adaptive change in rapidly radiating lineages. With these refined relationships, we resolve a long-standing debate about the origins of the races within each species, supporting the hypothesis that the red-rayed Amazonian pattern evolved recently and expanded, causing disjunctions of more ancestral patterns.Müllerian mimicry | population genetics | phylogeography R esearchers typically rely on neutrally evolving loci to generate a phylogenetic and population genetic history of adaptive divergence. The rationale is that these markers provide an unbiased view of the relationships among divergent phenotypes and a better understanding of the evolutionary processes generating variation. However, the genome is a complicated mosaic shaped by an interplay of mutation, drift, selection, and recombination. Recombination allows different regions of the genome to experience alternative restrictions to gene flow, and thus develop different evolutionary trajectories. The closer a genetic marker is to the alleles responsible for adaptive differences, the more likely that it will trace the history of phenotypic change.Understanding how phenotypic variation is generated in nature is greatly enhanced by studying groups that are actively undergoing diversification. By deciphering the history of such diverse phenotypes we gain a clearer understanding of the evolutionary process, including the tempo and mode of phenotypic change. Heliconius butterflies present one of the most striking examples of a recent phenotypic radiation. The 40 species in the genus exhibit hundreds of wing patterns that are involved in Müllerian mimicry complexes, where distasteful species converge on a shared warning signal to avoid predation. Th...

Avoidance of an aposematically coloured butterfly by wild birds in a tropical forest

“…Artificial butterflies were produced based on wings of Heliconius erato lativitta (Linnaeus) which is found only in the Amazon basin, not in Panama (Brown, 1979; Hines et al , 2011). We calibrated the appearance of the artificial wings to account for bird colour and luminance vision.…”

Repeated evolution in overlapping mimicry rings among North American velvet ants

“…Although Heliconius mimicry rings have become the most widely known mimetic systems due to the variety of shared colour forms found in apparently distantly related species and populations 2,5 , recent analyses suggest that some phenotypes share a common origin within and between species 29 . These recent findings indicate that mimetic races within Heliconius species may be driven in part by shared phylogenetic history in addition to convergent evolution.…”

Influences of geographic differentiation in the forewing warning signal of the wood tiger moth in Alaska

“…Investigations into the phylogeography of several aposematic species have revealed that current or historic barriers to gene flow may impact warning signal diversity (e.g., , Owen et al 1994, Turner & Mallet 1996, Noonan & Gaucher 2006, Hines et al 2011, Gehara et al 2013, Hill et al 2013. Over the course of the late Holocene glacial cycles influenced the biota of northern and tropical regions.…”