Flight was a key innovation in the adaptive radiation of insects. However, it is a complex trait influenced by a large number of interacting biotic and abiotic factors, making it difficult to unravel ...the evolutionary drivers. We investigate flight patterns in neotropical heliconiine butterflies, well known for mimicry of their aposematic wing color patterns. We quantify the flight patterns (wing beat frequency and wing angles) of 351 individuals representing 29 heliconiine and 9 ithomiine species belonging to ten color pattern mimicry groupings. For wing beat frequency and up wing angles, we show that heliconiine species group by color pattern mimicry affiliation. Convergence of down wing angles to mimicry groupings is less pronounced, indicating that distinct components of flight are under different selection pressures and constraints. The flight characteristics of the Tiger mimicry group are particularly divergent due to convergence with distantly related ithomiine species. Predator-driven selection for mimicry also explained variation in flight among subspecies, indicating that this convergence can occur over relatively short evolutionary timescales. Our results suggest that the flight convergence is driven by aposematic signaling rather than shared habitat between comimics. We demonstrate that behavioral mimicry can occur between lineages that have separated over evolutionary timescales ranging from <0.5 to 70 My.
Abstract
What drives the evolution of plumage color in birds? Bird color is likely to be under both natural and sexual selection where natural selection may favor evolution toward crypsis or ...camouflage whereas sexual selection may favor evolution toward conspicuousness. The responses to selection are predicted to relate to species’ ecology, behavior, and life history. Key hypotheses have focused on habitat and light environment, breeding strategy, territoriality, and hunting behavior. We tested these potential causes of color variation in the Coraciiformes, a colorful clade of non-passerine birds, using phylogenetic comparative methods and data on chromatic and achromatic properties of plumage coloration measured from museum specimens. We found that correlates of color evolution in Coraciiformes vary across body regions and depend on the focal color property (chromatic or achromatic properties of plumage coloration). While the light environment showed widespread effects on coloration in multiple body regions for both color properties, selection pressures related to behavioral characteristics had more spatially localized effects (e.g. territoriality on achromatic properties of wing feathers and hunting strategy on chromatic properties of belly feathers). Our results reveal both general patterns that may hold across other bird clades and more nuanced effects of selection that are likely to be mediated through the visual ecology of the signaler and receiver and the behavioral characteristics of Coraciiform species.
Comparing plumage color across species of kingfishers and their relatives, we show that habitat lighting conditions are an important factor shaping bird coloration. Differences in species behavior and ecology had more localized effects on particular body regions, with wing brightness evolving in response to territoriality and belly color being influenced by hunting strategy.
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.
The extravagant plumage traits of male birds are a favourite example of sexual selection. However, to date the units that selection is acting upon, the genes themselves have been a 'black box'. Here, ...we report evidence of change driven by sexual selection at a pigmentation gene locus in the galliform birds. Across species, we find a correlation between the rate of amino acid change (dN/dS) at this locus (MC1R) and the degree of sexual dichromatism, which we use as a measure of the strength of sexual selection. There is no evidence for a similar pattern in any of five other loci (four candidate and one control locus). This is consistent with previous work on colour polymorphisms and suggests that MC1R may be a key target for selection acting on plumage colour. The pattern of selection at MC1R seems to be consistent with the continuous or cyclical evolution of traits and preferences that is the outcome of several Fisherian and good-genes models of sexual selection. In contrast, we found no support for models of sexual selection that predict an increase in purifying selection as a result of purging of deleterious mutations or for models that predict an increased rate of mutation in association with stronger sexual selection.
Understanding how organisms adapt to their local environment is central to evolution. With new whole‐genome sequencing technologies and the explosion of data, deciphering the genomic basis of complex ...traits that are ecologically relevant is becoming increasingly feasible. Here, we studied the genomic basis of wing shape in two Neotropical butterflies that inhabit large geographical ranges. Heliconius butterflies at high elevations have been shown to generally have rounder wings than those in the lowlands. We reared over 1,100 butterflies from 71 broods of H. erato and H. melpomene in common‐garden conditions and showed that wing aspect ratio, that is, elongatedness, is highly heritable in both species and that elevation‐associated wing aspect ratio differences are maintained. Genome‐wide associations with a published data set of 666 whole genomes from across a hybrid zone, uncovered a highly polygenic basis to wing aspect ratio variation in the wild. We identified several genes that have roles in wing morphogenesis or wing aspect ratio variation in Drosophila flies, making them promising candidates for future studies. There was little evidence for molecular parallelism in the two species, with only one shared candidate gene, nor for a role of the four known colour pattern loci, except for optix in H. erato. Thus, we present the first insights into the heritability and genomic basis of within‐species wing aspect ratio in two Heliconius species, adding to a growing body of evidence that polygenic adaptation may underlie many ecologically relevant traits.
Iridescence is an optical phenomenon whereby colour changes with the illumination and viewing angle. It can be produced by thin film interference or diffraction. Iridescent optical structures are ...fairly common in nature, but relatively little is known about their production or evolution. Here we describe the structures responsible for producing blue-green iridescent colour in Heliconius butterflies. Overall the wing scale structures of iridescent and non-iridescent Heliconius species are very similar, both having longitudinal ridges joined by cross-ribs. However, iridescent scales have ridges composed of layered lamellae, which act as multilayer reflectors. Differences in brightness between species can be explained by the extent of overlap of the lamellae and their curvature as well as the density of ridges on the scale. Heliconius are well known for their Müllerian mimicry. We find that iridescent structural colour is not closely matched between co-mimetic species. Differences appear less pronounced in models of Heliconius vision than models of avian vision, suggesting that they are not driven by selection to avoid heterospecific courtship by co-mimics. Ridge profiles appear to evolve relatively slowly, being similar between closely related taxa, while ridge density evolves faster and is similar between distantly related co-mimics.
ASIP is an important pigmentation gene responsible for dorsoventral and hair-cycle-specific melanin-based color patterning in mammals. We report some of the first evidence that the avian ASIP gene ...has a role in pigmentation. We have characterized the genetic basis of the homozygous lethal Japanese quail yellow mutation as a >90-kb deletion upstream of ASIP. This deletion encompasses almost the entire coding sequence of two upstream loci, RALY and EIF2B, and places ASIP expression under control of the RALY promoter, leading to the presence of a novel transcript. ASIP mRNA expression was upregulated in many tissues in yellow compared to wild type but was not universal, and consistent differences were not observed among skins of yellow and wild-type quail. In a microarray analysis on developing feather buds, the locus with the largest downregulation in yellow quail was SLC24A5, implying that it is regulated by ASIP. Finally, we document the presence of ventral skin-specific isoforms of ASIP mRNA in both wild-type quails and chickens. Overall, there are remarkable similarities between yellow in quail and lethal yellow in mouse, which involve a deletion in a similar genomic position. The presence of ventral-specific ASIP expression in birds shows that this feature is conserved across vertebrates.
Theoretical models suggest that traits under divergent ecological selection, which also contribute to assortative mating, will facilitate speciation with gene flow. Evidence for these so‐called ...“magic traits” now exists across a range of taxa. However, their importance during speciation will depend on the extent to which they contribute to reproductive isolation. Addressing this requires experiments to determine the exact cues involved as well as estimates of assortative mating in the wild. Heliconius butterflies are well known for their diversity of bright warning color patterns, and their amenability to experimental manipulation has provided an excellent opportunity to test their role in reproductive isolation. Here, we reveal that divergent color patterns contribute to mate recognition between the incipient species Heliconius himera and H. erato, a taxon pair for which assortative mating by color pattern has been demonstrated among wild individuals: First, we demonstrate that males are more likely to attempt to mate conspecific females; second, we show that males are more likely to approach pinned females that share their own warning pattern. These data are valuable as these taxa likely represent the early stages of speciation, but unusually also allow comparisons with rates of interbreeding between divergent ecologically relevant phenotypes measured in the wild.
Theoretical models suggest that traits under divergent ecological selection, which also contribute to assortative mating, will facilitate speciation with gene flow. Divergent color patterns contribute to mate recognition between the incipient species Heliconius himera and H. erato, a taxon pair for which assortative mating by color pattern has been demonstrated among wild individuals.
Heliconius butterflies are an excellent system for studies of adaptive convergent and divergent phenotypic traits. Wing colour patterns are used as signals to both predators and potential mates and ...are inherited in a Mendelian manner. The underlying genetic mechanisms of pattern formation have been studied for many years and shed light on broad issues, such as the repeatability of evolution. In Heliconius melpomene, the yellow hindwing bar is controlled by the HmYb locus. MicroRNAs (miRNAs) are important post-transcriptional regulators of gene expression that have key roles in many biological processes, including development. miRNAs could act as regulators of genes involved in wing development, patterning and pigmentation. For this reason we characterised miRNAs in developing butterfly wings and examined differences in their expression between colour pattern races.
We sequenced small RNA libraries from two colour pattern races and detected 142 Heliconius miRNAs with homology to others found in miRBase. Several highly abundant miRNAs were differentially represented in the libraries between colour pattern races. These candidates were tested further using Northern blots, showing that differences in expression were primarily due to developmental stage rather than colour pattern. Assembly of sequenced reads to the HmYb region identified hme-miR-193 and hme-miR-2788; located 2380 bp apart in an intergenic region. These two miRNAs are expressed in wings and show an upregulation between 24 and 72 hours post-pupation, indicating a potential role in butterfly wing development. A search for miRNAs in all available H. melpomene BAC sequences (~2.5 Mb) did not reveal any other miRNAs and no novel miRNAs were predicted.
Here we describe the first butterfly miRNAs and characterise their expression in developing wings. Some show differences in expression across developing pupal stages and may have important functions in butterfly wing development. Two miRNAs were located in the HmYb region and were expressed in developing pupal wings. Future work will examine the expression of these miRNAs in different colour pattern races and identify miRNA targets among wing patterning genes.
Bright, highly reflective iridescent colours can be seen across nature and are produced by the scattering of light from nanostructures.
butterflies have been widely studied for their diversity and ...mimicry of wing colour patterns. Despite iridescence evolving multiple times in this genus, little is known about the genetic basis of the colour and the development of the structures which produce it.
can be found across Central and South America, but only races found in western Ecuador and Colombia have developed blue iridescent colour. Here, we use crosses between iridescent and non-iridescent races of
to study phenotypic variation in the resulting F
generation. Using measurements of blue colour from photographs, we find that iridescent structural colour is a quantitative trait controlled by multiple genes, with strong evidence for loci on the Z sex chromosome. Iridescence is not linked to the Mendelian colour pattern locus that also segregates in these crosses (controlled by the gene
). Small-angle X-ray scattering data show that spacing between longitudinal ridges on the scales, which affects the intensity of the blue reflectance, also varies quantitatively in F
crosses.
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