Mathematical modeling of the eyespots in butterfly wings. (21st December 2021)

• Record Type: Journal Article
• Authors: Liao, Kang-Ling; Chang, Wei-Chen; Marcus, Jeffrey M.; Wang, Jenn-Nan
• Is Part Of: Journal of theoretical biology. Volume 531(2021)
• Publication Date: 2021-12-21
• Subjects: Butterfly wings -- Pattern formation -- Reaction-diffusion model -- Gene expression; Biology -- Periodicals; Biological Science Disciplines -- Periodicals; Biology -- Periodicals; Biologie -- Périodiques; Theoretische biologie; Biology; Periodicals; 571.05
• DOI: 10.1016/j.jtbi.2021.110898
• Languages: English
• ISSNs: 0022-5193

Abstract

Highlights: PDE model based on gene regulation for eyespot formation in butterflies. Interaction among genes En, Hh, Ci, TGF-beta, and Wg. Deficiency of these genes induces degenerated eyespot patterns. Abstract: Butterfly wing color patterns are a representative model system for studying biological pattern formation, due to their two-dimensional simple structural and high inter- and intra-specific variabilities. Moreover, butterfly color patterns have demonstrated roles in mate choice, thermoregulation, and predator avoidance via disruptive coloration, attack deflection, aposematism, mimicry, and masquerade. Because of the importance of color patterns to many aspects of butterfly biology and their apparent tractability for study, color patterns have been the subjects of many attempts to model their development. Early attempts focused on generalized mechanisms of pattern formation such as reaction-diffusion, diffusion gradient, lateral inhibition, and threshold responses, without reference to any specific gene products. As candidate genes with expression patterns that resembled incipient color patterns were identified, genetic regulatory networks were proposed for color pattern formation based on gene functions inferred from other insects with wings, such as Drosophila . Particularly detailed networks incorporating the gene products, Distal-less (Dll), Engrailed (En), Hedgehog (Hh), Cubitus interruptus (Ci), Transforming growth factor- β (TGF- β ), and Wingless (Wg), have been proposed for butterfly border ocelli (eyespots) which helps the investigation of the formation of these patterns. Thus, in this work, we develop a mathematical model including the gene products En, Hh, Ci, TGF- β, and Wg to mimic and investigate the eyespot formation in butterflies. Our simulations show that the level of En has peaks in the inner and outer rings and the level of Ci has peaks in the inner and middle rings. The interactions among these peaks activate cells to produce white, black, and yellow pigments in the inner, middle, and outer rings, respectively, which captures the eyespot pattern of wild type Bicyclus anynana butterflies. Additionally, our simulations suggest that lack of En generates a single black spot and lack of Hh or Ci generates a single white spot, and a deficiency of TGF- β or Wg will cause the loss of the outer yellow ring. These deficient patterns are similar to those observed in the eyespots of Vanessa atalanta, Vanessa altissima, and Chlosyne nycteis . Thus, our model also provides a hypothesis to explain the mechanism of generating the deficient patterns in these species.