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. K E Y W O R D S : Altitude, Heliconius, Lepidoptera, phenotypic divergence, sexual dimorphism, wing morphology.

Microclimate buffering and thermal tolerance across elevations in a tropical butterfly

“…Every Heliconius species encountered at each site was collected, but only those species with more than 5 individuals at each elevation (high and/or low) were included in the analyses (15 out of 329 wild individuals removed). Detached wings were photographed dorsally and ventrally with a DSLR camera with a 100 mm macro lens in standardised conditions, and wing area was measured with an automated pipeline in the public software Fiji (following Montejo-Kovacevich et al, 2019). Butterflies with Heliconius melpomene malleti phenotypes were genotyped with a restriction digest of amplified COI genes (following Nadeau et al, 2014), to identify cryptic H. timareta spp.…”

“…Offspring from high and low altitude mothers had individual IDs with no indication of their origin, thus we were able to blindly test five individuals at a time and avoid potential observer bias. Adult offspring wings were photographed and their wing areas measured with an automated pipeline in the open-access software Fiji (following Montejo-Kovacevich et al, 2019).…”

“…Behavioural shifts might alleviate the impact of climate extremes in tropical forests, but the capacity of a species to shift sufficiently will be constrained by life history, energy budgets, and thermal tolerance (Sheldon and Tewksbury, 2014). In these butterflies, altitude has been shown to pose strong selective pressures, and some are constrained in their body size by contrasting reproductive strategies (gregarious vs. solitary), which could, in turn, restrict adaptive plastic responses to environmental change (Montejo-Kovacevich et al, 2019). Nevertheless, the observed thermal buffering of forests would undoubtedly benefit and be exploited by these butterflies during extreme temperature events, such as the 31 days where temperatures in the lowlands went above 39C.…”

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, ). 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, ). In Heliconius butterflies, Müller () 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.…”

Microclimate buffering and thermal tolerance across elevations in a tropical butterfly

“…Every Heliconius species encountered at each site was collected, but only those species with more than 5 individuals at each elevation (high and/or low) were included in the analyses (15 out of 329 wild individuals removed). Detached wings were photographed dorsally and ventrally with a DSLR camera with a 100 mm macro lens in standardised conditions, and wing area was measured with an automated pipeline in the public software Fiji (following Montejo-Kovacevich et al, 2019). All the images are available in the public repository Zenodo (https://zenodo.org/communities/butterfly/) and full records with data are stored in the EarthCape database (https://heliconius.ecdb.io).…”