The development and

evolution of wing patterns

 
 

This research has focussed on the development and evolution of pigment patterns in butterflies. Butterfly wing patterns are particularly interesting for the study of pattern formation because they are perfectly two-dimensional (each wing surface is made by a monolayer of cells, and there is no cell migration or rearrangement during pattern formation), and the pattern consists of the localized synthesis of pigments whose chemical structure and synthetic pathways are reasonably well understood. Our early research on this system demonstrated that the overall pattern is made up of a discrete set of semi-independent pattern elements. The identity of each pattern element can be traced from species to species, and often across genera and families. The pattern elements of butterfly wings are individuated and admit to a system of homologies that is as reliable as those of the bones of the vertebrate skeleton.

Evolution of the overall wing pattern occurs by distorting and displacing these pattern elements, by changing their pigmentation, and by selectively suppressing or enlarging specific elements. The genetic and phenotypic covariances between pattern elements and between different aspects of a pattern element (such as position and size) are very small or zero. These low covariances are due to developmental uncoupling of pattern elements. This produces a system in which there are relatively few developmental constraints on variation and evolution, and this may account for the enormous diversity of color patterns in this group.

Recent studies have dealt with the genetics of mimicry in Papilio dardanus. This large African butterfly has a sex-limited polymorphic mimicry. That is to say, only the females are mimics, and they mimic several very different-looking species of unpalatable danaid butterflies. This mimicry is controlled by alternative alleles at a single locus. Ten alleles are known (from Mendelian studies), and most of them give perfect mimicry to a different species of butterfly. Together with a team, funded by the Human Frontier Science Program, investigated how it is possible for allelic variation at a single gene to produce phenotypes that are perfect mimics of different species. (In a sense, this complements our work on polyphenic development, where we study how alternative phenotypes are produced without any genetic differences whatsoever).

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The Nymphalid Groundplan

The Nymphalid groundplan is a representation of the relationships among the elements of the color patterns of butterflies. As its name implies, it applies strictly only to the family Nymphalidae (s.l.), but it turns out to be useful also for understanding the structure of the color patterns of other butterflies and many moths.

 
 
 

 

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The color patterns of butterflies are based on three systems of bands, called symmetry systems (the basal, central, and border symmetry systems).

In its primitive form, the bands of the symmetry system run smoothly and uninterrupted from the anterior to the posterior margins of the wing. This is the patterning system the butterflies inherited from their moth ancestors.

In butterflies, the border symmetry system often bears small eyespots, the border ocelli (bo). In some species these are modified into large eyespots that are believed to startle or confuse potential predators. The large eyespots in moths are usually modifications of the discal spot (d).

 
    The color patterns of butterflies are compartmentalized by the wing veins.

Each compartment is developmentally isolated from its neighbors during pattern determination.

The consequence of this is that pattern development in each compartment becomes semi-independent from that of its neighbors.

This results in a dislocation of the symmetry system bands where they cross wing veins.

The patterns of the thousands of species of butterflies are derived from this groundplan by selectively suppressing the development of individual pattern elements, by distorting their shape, by enlarging them, by moving them about on the wing, and by changing their color.

 
       
The Nymphalid Groundplan can give rise to two classes of very different-looking patterns that I call Detailed Patterns and Bold Patterns. The former are most commonly (but not exclusively) found on the ventral wing surfaces and often serve to camouflage, while the latter or most commonly found of the dorsal wing surfaces and typically are used for territorial, mating and aposematic displays.
 
 
   

Below are a set of animations that illustrate how different color patterns are derived from the Nymphalid Groundplan (these are flash movies (*.flv) and you may need to install a flash viewer to see them).

This first set shows the derivation of Detailed Patterns of three species of nymphalid butterflies.

   
Stichophtalma camadeva
 
Precis (junonia) coenia  

 

Kallima inachus (watch how the "midrib" is derived)  
     
 
 

 

The next set of animations shows the derivation of several Bold Patterns of Heliconius butterflies from the Groundplan.

 
 

Derivation of the Heliconius groundplan is based on comparative studies of the so-called sylvaniform patterns, which illustrate clearly how the pattern elements of the Nymphalid Groundplan move, expand and fuse to form large and irregular areas of black pattern on a colored background.

Sylvaniform patterns

The Heliconius Groundplan

   
Heliconius erato petiverana
Heliconious melpomene aglaope
Heliconius charitonia
Heliconius cydno pachinus
 

 

Some references to our work

Nijhout, H.F., 1991, The Development and Evolution of Butterfly Wing Patterns, Smithsonian Institution Press, Washington, D.C.

 

Reed R.D., Chen P.H. and Nijhout, H.F. 2007.. Cryptic variation in butterfly eyespot development: the importance of sample size in gene expression studies. Evolution & Development 9: 2-9.

Nijhout, H.F. 2006. Stochastic gene expression: dominance, thresholds and boundaries. In: Dominance and Haploinsufficiency (R.A. Veitia, Ed.).pp. 61-75. Landes Press.

Veitia, R. and Nijhout, H.F. 2006. The robustness of the transcriptional response to alterations in morphogenetic gradients. BioEssays 28: 282-289.

Nijhout, H.F. 2003.  polymorphic mimicry in Papilio dardanus: mosaic dominance, big effects, and origins.  Evolution & Development 5: 579-582. (PDF)

Nijhout, H.F. 2003. Gradients, diffusion and genes in pattern formation. In: Origination of Organismal Form (G. Müller and S. Newman, eds.), pp. 165-181. MIT Press.

Koch, P.B. and H.F. Nijhout. 2002. The role of wing veins in colour pattern development in the butterfly Papilio xuthus (Lepidoptera: Papilionidae). European Journal of Entomology 99: 67-72.

Nijhout, H.F. 2001. Origin of butterfly wing patterns. In: The Character Concept in Evolutionary Biology. (G.A. Wagner ed.), pp. 511-529. Academic Press.

Nijhout, H.F. 2001. Elements of Butterfly Wing Patterns. J. Exp. Zool. (Molec. Evol. and Dev.) 291: 213-225. (PDF)

Miner, A.L., A.J. Rosenberg and H.F. Nijhout. 2000. Control of growth and differentiation of the wing imaginal disks of Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 46: 251-258.

Weatherbee, S.D., H. F. Nijhout, L.W. Grunert, G. Halder, R. Galant, J. Selegue, and S. Carroll. 1999. Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Current Biology 9: 109-115.(PDF)

Nijhout, H.F. 1997. Ommochrome pigmentation of the linea and rosa seasonal forms of Precis coenia (Lepidoptera: Nymphalidae). Arch. Insect Biochem. Physiol. 36: 215-222. (PDF)

Nijhout, H.F. 1996. Focus on butterfly eyespot development. Nature 384:209-210.

Rountree, D.B. and H. F. Nijhout. 1995. Genetic control of a seasonal morph in Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 41:1141-1145.

Rountree, D.B. and H. F. Nijhout. 1995. Hormonal control of a seasonal polyphenism in Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 41:987-992

Nijhout, H.F. and D.B. Rountree. 1995. Pattern induction across a homeotic boundary in the wings of Precis coenia (Lepidoptera: Nymphalidae). Int. J. Insect Morphol. Embryol. 24: 243-251.

Nijhout, H.F., 1994. Symmetry systems and compartments in Lepidopteran wings: The evolution of a patterning system. Development ( 1994 Suppl.): 225-233.

Nijhout, H.F., 1994. Developmental perspectives on evolution of mimicry in butterflies. BioScience 44:148-157.

Nijhout, H.F., 1994. Genes on the wing. Science 265:44-45.

Nijhout, H.F., G.A. Wray and L.E. Gilbert, 1990, An analysis of the phenotypic effects of certain color pattern genes in Heliconius. Biol. J. Linn. Soc. 40:357-372.

Nijhout, H.F., 1990, A comprehensive model for color pattern formation in butterflies. Proc. Roy. Soc. B 239:81-113.

Nijhout, H.F. and L.W. Grunert, 1988, Colour pattern regulation after surgery on the wing disks of Precis coenia (Lepidoptera: Nymphalidae). Development 102:337-385.

Nijhout, H.F. and G.A. Wray, 1988, Homologies in the color patterns of the genus Heliconius (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 33:345-365.

Nijhout, H.F. and G.A. Wray, 1986, Homologies in the colour patterns of the genus Charaxes (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 28:387-410.

Nijhout, H.F., 1985, Cautery induced colour patterns in Precis coenia (Lepidoptera: Nymphalidae). J. Embryol. Exp. Morphol. 86:191-203.

Nijhout, H.F., 1985, Independent development of homologous pattern elements in the wing patterns of butterflies. Dev. Biol. 108:146-151.

Nijhout, H.F., 1985, The developmental physiology of colour patterns in lepidoptera. Adv. Insect Physiol. 18:181- 247.

Nijhout, H.F., 1984, Colour pattern modification by coldshock in Lepidoptera. J. Embryol. Exp. Morphol. 18:287-305.

Nijhout, H.F., 1980, Pattern formation on lepidopteran wings: Determination of an eyespot. Develop. Biol. 80:267-274.

Nijhout, H.F., 1980, Ontogeny of the color pattern on the wings of Precis coenia (Lepidoptera, Nymphalidae). Develop. Biol. 80:275-288.