Some genes have repeatedly been found to control diverse adaptations in a wide variety of organisms. Such gene reuse reveals not only the diversity of phenotypes these unique genes control but also the composition of developmental gene networks and the genetic routes available to and taken by organisms during adaptation. However, the causes of gene reuse remain unclear. A small number of large-effect Mendelian loci control a huge diversity of mimetic butterfly wing color patterns, but reasons for their reuse are difficult to identify because the genetic basis of mimicry has primarily been studied in two systems with correlated factors: female-limited Batesian mimicry in Papilio swallowtails (Papilionidae) and non-sex-limited Müllerian mimicry in Heliconius longwings (Nymphalidae). Here, we break the correlation between phylogenetic relationship and sex-limited mimicry by identifying loci controlling female-limited mimicry polymorphism Hypolimnas misippus (Nymphalidae) and non-sex-limited mimicry polymorphism in Papilio clytia (Papilionidae). The Papilio clytia polymorphism is controlled by the genome region containing the gene cortex, the classic P supergene in Heliconius numata, and loci controlling color pattern variation across Lepidoptera. In contrast, female-limited mimicry polymorphism in Hypolimnas misippus is associated with a locus not previously implicated in color patterning. Thus, although many species repeatedly converged on cortex and its neighboring genes over 120 My of evolution of diverse color patterns, female-limited mimicry polymorphisms each evolved using a different gene. Our results support conclusions that gene reuse occurs mainly within ∼10 My and highlight the puzzling diversity of genes controlling seemingly complex female-limited mimicry polymorphisms.
The Evolution of Color Pattern in Butterflyfishes (Chaetodontidae)
Abstract Coral reef fishes constitute one of the most diverse assemblages of vertebrates on the planet. Color patterns are known to serve a number of functions including intra- and inter-specific signaling, camouflage, mimicry, and defense. However, the relative importance of these and other factors in shaping color pattern evolution is poorly understood. Here we conduct a comparative phylogenetic analysis of color pattern evolution in the butterflyfishes (Chaetodontidae). Using recently developed tools for quantifying color pattern geometry as well as machine learning approaches, we investigate the tempo of evolution of color pattern elements and test whether ecological variables relating to defense, depth, and social behavior predict color pattern evolution. Butterflyfishes exhibit high diversity in measures of chromatic conspicuousness and the degrees of fine versus gross scale color patterning. Surprisingly, most diversity in color pattern was not predicted by any of the measures of ecology in our study, although we did find a significant but weak relationship between the level of fine scale patterning and some aspects of defensive morphology. We find that the tempo of color pattern diversification in butterflyfishes has increased toward the present and suggest that rapid evolution, presumably in response to evolutionary pressures surrounding speciation and lineage divergence, has effectively decoupled color pattern geometry from some aspects of ecology. Machine learning classification of color pattern appears to rely on a set of features that are weakly correlated with current color pattern geometry descriptors, but that may be better suited for the detection of discrete components of color pattern. A key challenge for future studies lies in determining whether rapid evolution has generally decoupled color patterns from ecology, or whether convergence in function produces convergence in color pattern at phylogenetic scales.
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- Award ID(s):
- 1839250
- NSF-PAR ID:
- 10170986
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 3
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 604 to 615
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
null (Ed.)Abstract Background Heliconius butterflies are widely distributed across the Neotropics and have evolved a stunning array of wing color patterns that mediate Müllerian mimicry and mating behavior. Their rapid radiation has been strongly influenced by hybridization, which has created new species and allowed sharing of color patterning alleles between mimetic species pairs. While these processes have frequently been observed in widespread species with contiguous distributions, many Heliconius species inhabit patchy or rare habitats that may strongly influence the origin and spread of species and color patterns. Here, we assess the effects of historical population fragmentation and unique biology on the origins, genetic health, and color pattern evolution of two rare and sparsely distributed Brazilian butterflies, Heliconius hermathena and Heliconius nattereri . Results We assembled genomes and re-sequenced whole genomes of eight H. nattereri and 71 H. hermathena individuals. These species harbor little genetic diversity, skewed site frequency spectra, and high deleterious mutation loads consistent with recent population bottlenecks. Heliconius hermathena consists of discrete, strongly isolated populations that likely arose from a single population that dispersed after the last glacial maximum. Despite having a unique color pattern combination that suggested a hybrid origin, we found no genome-wide evidence that H. hermathena is a hybrid species. However, H. hermathena mimicry evolved via introgression, from co-mimetic Heliconius erato , of a small genomic region upstream of the color patterning gene cortex . Conclusions Heliconius hermathena and H. nattereri population fragmentation, potentially driven by historical climate change and recent deforestation, has significantly reduced the genetic health of these rare species. Our results contribute to a growing body of evidence that introgression of color patterning alleles between co-mimetic species appears to be a general feature of Heliconius evolution.more » « less
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Copenhaver, Gregory P. (Ed.)Patterns of genomic architecture across insects remain largely undocumented or decoupled from a broader phylogenetic context. For instance, it is unknown whether translocation rates differ between insect orders. We address broad scale patterns of genome architecture across Insecta by examining synteny in a phylogenetic framework from open-source insect genomes. To accomplish this, we add a chromosome level genome to a crucial lineage, Coleoptera. Our assembly of the Pachyrhynchus sulphureomaculatus genome is the first chromosome scale genome for the hyperdiverse Phytophaga lineage and currently the largest insect genome assembled to this scale. The genome is significantly larger than those of other weevils, and this increase in size is caused by repetitive elements. Our results also indicate that, among beetles, there are instances of long-lasting (>200 Ma) localization of genes to a particular chromosome with few translocation events. While some chromosomes have a paucity of translocations, intra-chromosomal synteny was almost absent, with gene order thoroughly shuffled along a chromosome. This large amount of reshuffling within chromosomes with few inter-chromosomal events contrasts with patterns seen in mammals in which the chromosomes tend to exchange larger blocks of material more readily. To place our findings in an evolutionary context, we compared syntenic patterns across Insecta in a phylogenetic framework. For the first time, we find that synteny decays at an exponential rate relative to phylogenetic distance. Additionally, there are significant differences in decay rates between insect orders, this pattern was not driven by Lepidoptera alone which has a substantially different rate.more » « less
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Abstract Antipredatory displays that incorporate hidden contrasting coloration are found in a variety of different animals. These displays are seen in organisms that have drab coloration at rest, but when disturbed reveal conspicuous coloration. Examples include the bright abdomens of mountain katydids and the colorful underwings of hawk moths. Such hidden displays can function as secondary defenses, enabling evasion of a pursuant predator. To begin to understand why some species have these displays while others do not, we conducted phylogenetic comparative analyses to investigate factors associated with the evolution of hidden contrasting coloration in leaf‐footed bugs. First, we investigated whether hidden contrasting coloration was associated with body size because these displays are considered to be more effective in larger organisms. We then investigated whether hidden contrasting coloration was associated with an alternative antipredatory defense, in this case rapid autotomy. We found that leaf‐footed bugs with hidden contrasting coloration tended to autotomize more slowly, but this result was not statistically significant. We also found that the presence of a body size association was dependent upon the form of the hidden color display. Leaf‐footed bugs that reveal red/orange coloration were the same size, on average, as species without a hidden color display. However, species that reveal white patches on a black background were significantly larger than species without a hidden color display. These results highlight the diversity of forms that hidden contrasting color signal can take, upon which selection may act differently.
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null (Ed.)Abstract Background Bird plumage exhibits a diversity of colors that serve functional roles ranging from signaling to camouflage and thermoregulation. However, birds must maintain a balance between evolving colorful signals to attract mates, minimizing conspicuousness to predators, and optimizing adaptation to climate conditions. Examining plumage color macroevolution provides a framework for understanding this dynamic interplay over phylogenetic scales. Plumage evolution due to a single overarching process, such as selection, may generate the same macroevolutionary pattern of color variation across all body regions. In contrast, independent processes may partition plumage and produce region-specific patterns. To test these alternative scenarios, we collected color data from museum specimens of an ornate clade of birds, the Australasian lorikeets, using visible-light and UV-light photography, and comparative methods. We predicted that the diversification of homologous feather regions, i.e., patches, known to be involved in sexual signaling (e.g., face) would be less constrained than patches on the back and wings, where new color states may come at the cost of crypsis. Because environmental adaptation may drive evolution towards or away from color states, we tested whether climate more strongly covaried with plumage regions under greater or weaker macroevolutionary constraint. Results We found that alternative macroevolutionary models and varying rates best describe color evolution, a pattern consistent with our prediction that different plumage regions evolved in response to independent processes. Modeling plumage regions independently, in functional groups, and all together showed that patches with similar macroevolutionary models clustered together into distinct regions (e.g., head, wing, belly), which suggests that plumage does not evolve as a single trait in this group. Wing patches, which were conserved on a macroevolutionary scale, covaried with climate more strongly than plumage regions (e.g., head), which diversified in a burst. Conclusions Overall, our results support the hypothesis that the extraordinary color diversity in the lorikeets was generated by a mosaic of evolutionary processes acting on plumage region subsets. Partitioning of plumage regions in different parts of the body provides a mechanism that allows birds to evolve bright colors for signaling and remain hidden from predators or adapt to local climatic conditions.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icz119
