Altitude and life‐history shape the evolution ofHeliconiuswings

Abstract

Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal‐mating clade are smaller than those in the adult‐mating clade. Interestingly, we find that high‐altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high‐altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration.

Structures related to pheromone storage in alar androconia and the female abdominal scent gland of Heliconius erato phyllis, Heliconius ethilla narcaea, and Heliconius besckei (Lepidoptera: Nymphalidae: Heliconiinae)

“…Butterfly wing size varies according to the quality and quantity of the food source provided by larval host plants (Rodrigues & Moreira, 2004). It also varies according to the behavioral ecology of larvae and adults, as for example in lonely larvae, adults of the adult-mating clade and of higher altitudes, that have larger wings (Montejo-Kovacevich et al, 2019). In Heliconius butterflies, Müller (1912) showed through illustrations and text that the androconial scales of Heliconius apseudes (Hübner, [1813]), Heliconius eucrate (Godart, 1819) and Heliconius besckei Ménétriés, 1857, among other Nymphalidae, are quite variable on the upper surface of the hindwing, near the costal margin and particularly along the costal and subcostal veins.…”

Genomics of altitude-associated wing shape in two tropical butterflies

“…The amount of wing shape variation explained by family across common-garden reared offspring was high for both species (H. erato: 21% and H. melpomene: 39%), especially when compared to the 74% of variance explained by species identity in a previous comparative study (Montejo-Kovacevich et al, 2019). The resemblance in wing aspect ratio between mothers and their offspring is indicative of a highly heritable trait (Fig.…”

“…Generally, cases of wing shape plasticity are rarer than size plasticity, especially if the two traits are allometrically decoupled, allowing for subtle changes to be selected if advantageous (Carreira et al, 2011;Gilchrist & Partridge, 2001;Strauss, 1990). In Heliconius, wings have been found to be rounder at higher elevations, both across and within species that inhabit large ranges (Montejo-Kovacevich et al, 2019). In our study, wing shape differences observed in the wild in H. erato and H. melpomene were maintained in common-garden reared broods, with individuals from highland mothers having, on average, rounder wings (Fig.…”

“…Insect wing shape is phylogenetically conserved in many taxa (Houle, Mezey, Galpern, & Carter, 2003;Montejo-Kovacevich et al, 2019;Thomas, Walsh, Wolf, McPheron, & Marden, 2000), but also highly evolvable in the laboratory (Houle et al, 2003), suggesting that wing shape can be heritable. Wing shape tends to have higher heritability than wing size in flies and wasps (Gilchrist & Partridge, 2001;Klingenberg, Debat, & Roff, 2010;Xia, Pannebakker, Groenen, Zwaan, & Bijma, 2020), as size is more prone to life-history trade-offs and condition-dependency.…”

“…Here we study the genetic basis of wing shape variation in two widespread species of Heliconius butterflies across an elevational cline in the Ecuadorian Andes. Heliconius inhabiting high altitudes have recently been found to have rounder wings than lowland butterflies, a pattern seen both across species and within species along elevational clines (Montejo-Kovacevich et al, 2019). To estimate the heritability of this potentially adaptive trait, we common-garden reared 71 broods of H. erato lativitta and H. melpomene malleti from across the cline, yielding 1141 offspring (Fig.…”