Toshio Sekimura - Diversity and Evolution of Butterfly Wing Patterns: An Integrative Approach
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This book facilitates an integrative understanding of the development, genetics and evolution of butterfly wing patterns. To develop a deep and realistic understanding of the diversity and evolution of butterfly wing patterns, it is essential and necessary to approach the problem from various kinds of key research fields such as evo-devo, eco-devo, developmental genetics, ecology and adaptation, food plants, and theoretical modeling.The past decade-and-a-half has seen a veritable revolution in our understanding of the development, genetics and evolution of butterfly wing patterns. In addition, studies of how environmental and climatic factors affect the expression of color patterns has led to increasingly deeper understanding of the pervasiveness and underlying mechanisms of phenotypic plasticity. In recognition of the great progress in research on the biology, an international meeting titled Integrative Approach to Understanding the Diversity of ButterflyWing Patterns (IABP-2016) was held at Chubu University, Japan in August 2016. This book consists of selected contributions from the meeting. Authors include main active researchers of new findings of corresponding genes as well as world leaders in both experimental and theoretical approaches to wing color patterns.The book provides excellent case studies for graduate and undergraduate classes in evolution, genetics/genomics, developmental biology, ecology, biochemistry, and also theoretical biology, opening the door to a new era in the integrative approach to the analysis of biological problems.This book is open access under a CC BY 4.0 license.
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Anne Wanjie
Pam Holden
Karl J. Niklas
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Joanna R. Freeland
Kensal E. van Holde
Tom Jackson
George F. Michel
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Part I
The Nympalid Groundplan (NGP) and Diversification
The Nympalid Groundplan (NGP) and Diversification
The Author(s) 2017
Toshio Sekimura and H. Frederik Nijhout (eds.) Diversity and Evolution of Butterfly Wing Patterns1. The Common Developmental Origin of Eyespots and Parafocal Elements and a New Model Mechanism for Color Pattern Formation
H. Frederik Nijhout 1
(1)
Department of Biology, Duke University, Durham, NC 27708, USA
H. Frederik Nijhout
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Abstract
The border ocelli and adjacent parafocal elements are among the most diverse and finely detailed features of butterfly wing patterns. The border ocelli can be circular, elliptical, and heart-shaped or can develop as dots, arcs, or short lines. Parafocal elements are typically shaped like smooth arcs but are also often V, W, and M shaped. The fusion of a border ocellus with its adjacent parafocal element is a common response to temperature shock and treatment with chemicals such as heparin and tungstate ions. Here I develop a new mathematical model for the formation of border ocelli and parafocal elements. The models are a reaction-diffusion model based on the well-established gradient-threshold mechanisms in embryonic development. The model uses a simple biochemical reaction sequence that is initiated at the wing veins and from there spreads across the field in the manner of a grass-fire. Unlike Turing-style models, this model is insensitive to the size of the field. Like real developmental systems, the model does not have a steady state, but the pattern is read out at a point in development, in response to an independent developmental signal such as a pulse of ecdysone secretion, which is known to regulate color pattern in butterflies. The grass-fire model reproduces the sequence of Distal-less expression that determines the position of eyespot foci and also shows how a border ocellus and its neighboring parafocal element can arise from such a single focus. The grass-fire model shows that the apparent fusion of ocellus and parafocal element is probably due to a premature termination of the normal process that separates the two and supports the hypothesis that the parafocal element is the distal band of the border symmetry system.
Keywords
Mathematical model Eyespot Parafocal element Grass-fire model Temperature shock1.1 Introduction
The color patterns of butterflies are extremely diverse, and almost all of the 14,000 or so species can be identified on the basis of their color patterns alone. Adding to this diversity is the fact that dorsal and ventral color patterns are usually entirely different and that many species have polymorphic, sexually dimorphic, and seasonally plastic color patterns. The development and evolution of this diversity of patterns has been of considerable interest, particularly in relation to the genetics and evolution of mimicry (Reed et al. ).
The organizing principles of color patterns are coming to be increasingly well understood. The diversity of mimicry patterns in Heliconius butterflies is due to the variation in only a handful of genes (Nadeau ).
The developmental mechanism that produces the spatial pattern of pigments that characterizes color patterns is less well understood. It is clear, however, that the wing veins and the wing margin play critical roles in organizing the pattern. This evidence comes, among others, from observations of the color patterns of mutants that lack wing veins and from experimental manipulations that alter the wing margin (e.g., Fig. )). 
Fig. 1.1
Color pattern modification in the veinless mutant of Papilio xuthus ( right ), compared with the normal pattern ( left ). The longitudinal veins are missing and so are the venous patterns. The submarginal bands are smoothly continuous and parallel to the wing margin, suggesting that the wing margin also plays an important role in color pattern determination
1.2 Eyespots and Parafocal Elements
The color patterns of butterflies are organized as a set of three-symmetry systems (Sffert ). 
Fig. 1.2
The nymphalid ground plan showing three symmetry systems: basal, central, and border. The border symmetry system has border ocelli (bo) on the compartment midlines. These border ocelli can develop into elaborate eyespots but also into many other shapes. The shape of the distal band of the border symmetry system can also be very diverse, and this band is recognized as the parafocal element
The proximal and distal bands of the border symmetry system have very different characters. The proximal band, when present, is typically arc shaped, or nearly straight. The distal bands are almost always present and have an exceptionally diverse array of shapes. Because its development and evolution are quite independent of that of the border ocelli, this element has been given a special name: the parafocal element (Nijhout ). The parafocal elements are developmentally closely related to the border ocelli. Indeed the two are developmentally interdependent in that they appear to arise from a common determination mechanism, although the determinants of their shape are quite different.
1.3 Puzzling Results of Temperature Shock Experiments
A number of investigators have observed that when color pattern aberrations are induced by temperature shock and various chemicals, one of the commonly observed features is a partial or complete fusion of the ocellus and the parafocal element (Otaki in reverse order, then it would seem that a single pattern element breaks into two, with the distal one forming the parafocal element and the proximal one the ocellus. None of the current models of color pattern formation can account for this. 
Fig. 1.3
Fusion of ocelli and parafocal elements after temperature shock in Vanessa cardui . Top row , dorsal surface. Bottom row , ventral surface. Normal patterns are on the left in each row. Bottom row shows a moderately affected pattern in the middle, and a severely affected pattern in which both pattern elements are completely fused is on the right
1.4 Models of Color Pattern Formation
Previous models for color pattern formation in butterflies have shown that it must be a two-step process. The first step is the establishment of organizing centers, and the second step is the organization of patterns of pigment synthesis by signals produced by these organizing centers. The best known of these organizing centers is the focus, a group of cells that occurs at the center of a canonical eyespot. The foci express both notch and Distal-less, in succession (Carroll et al. ).
The mechanism that determines the placement of foci on the wing is still unknown. Foci always occur exactly on the midline of wing compartments delineated by wing veins (i.e., equidistant from the veins). Intervenous stripe patterns (e.g., Fig. ), suggesting a common developmental origin of stripes and spots.
Color pattern determination begins in the wing imaginal disk shortly after the wing venation system is established. The wing imaginal disk is composed of two cell layers, for the dorsal and ventral wing surfaces, respectively. The two cell layers are tightly adhered to each other via a basement membrane. Wing veins develop as tube-like separations between the two layers. The veins are continuous with the hemocoel and allow entry of hemolymph into the developing and growing wing. A special vein called the bordering lacuna (Nijhout ).
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