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The genetics and evo–devo of butterfly wing patterns

Key Points

  • Butterfly wings show a spectacular diversity of patterns of colours and shapes both within and among species.

  • Butterfly wing patterns are ideal systems for an integrated study of the reciprocal interactions between the evolutionary and developmental processes that shape morphology.

  • The evolutionary flexibility of butterfly wing patterns might be facilitated by the compartmentalization of pattern elements (such as eyespots and chevrons) in individual wing regions.

  • The 'nymphalid groundplan', a theoretical model that describes homologies among butterfly wing patterns on the basis of morphology, has been very useful to compare different patterns, but might not always reflect developmental homologies.

  • The mechanistic dissection of wing-pattern diversity has focused on the cellular components and genetic pathways that underlie eyespot formation.

  • Future work will need to integrate different aspects of these mechanisms in species from different taxa that have different wing patterns, and combine such studies with a more detailed ecological analysis in nature.

Abstract

Understanding how the spectacular diversity of colour patterns on butterfly wings is shaped by natural selection, and how particular pattern elements are generated, has been the focus of both evolutionary and developmental biologists. The growing field of evolutionary developmental biology has now begun to provide a link between genetic variation and the phenotypes that are produced by developmental processes and that are sorted by natural selection. Butterfly wing patterns are set to become one of the few examples of morphological diversity to be studied successfully at many levels of biological organization, and thus to yield a more complete picture of adaptive morphological evolution.

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Figure 1: Examples of model butterfly species.
Figure 2: The 'nymphalid groundplan'.
Figure 3: Wing-pattern mutants.
Figure 4: Gene expression in butterfly wing primordia.
Figure 5: Cellular basis of variation in eyespot morphology.

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Acknowledgements

We thank A. Monteiro, F. Nijhout and M. Serfas for comments on this manuscript, and M. Brittijn for figure 5. This work was supported by a grant from the Human Frontier Science Program.

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Correspondence to Patrícia Beldade or Paul M. Brakefield.

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DATABASES

Achaete-scute Complex

apterous

cubitus interruptus

decapentaplegic

Delta

Distal-less

engrailed

hedgehog

patched

spalt

Ultrabithorax

wingless

FURTHER INFORMATION

Section of Evolutionary Biology, University of Leiden

Glossary

PHENOTYPIC PLASTICITY

The variation in phenotype of a given genotype when the individuals complete their development in different environments.

APOSEMATIC

Describes a conspicuous colour pattern that is associated with venomous or distasteful prey and serves as a warning signal to potential predators.

CRYPSIS

The property of those colour patterns that resemble the background as perceived by predators that hunt by sight. Cryptic individuals are well camouflaged.

SEXUAL SELECTION

The selection that results from differential mating success. It includes competition for mates (usually among males) and mate choice (usually by females).

IMAGINAL DISC

Sac-like infolding of the epithelium in the larva. They give rise to most of the external structures of the adult. Imaginal disc cells are set aside in the embryo and continue to divide until pupation, when they differentiate.

ADDITIVE GENETIC VARIANCE

The genetic variance that can be statistically associated with the linear relationship between mean offspring and mid-parent values. This is the component of variance that contributes to the response to selection.

HERITABILITY

The proportion of the total phenotypic variation in a given characteristic that can be attributed to additive genetic effects.

RNA INTERFERENCE

(RNAi). A process by which double-stranded RNA specifically silences the expression of homologous genes through interference with their cognate mRNA.

MORPHOLINO

A chemically modified oligonucleotide that behaves as an antisense RNA analogue and is therefore used to interfere with gene function.

GENETIC ARCHITECTURE

This term broadly describes the distribution of gene effects that produce a given phenotype. It includes a description of the number of genes that influence the trait, the relative position and magnitude of the effects, and the nature of the interactions between them.

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Beldade, P., Brakefield, P. The genetics and evo–devo of butterfly wing patterns. Nat Rev Genet 3, 442–452 (2002). https://doi.org/10.1038/nrg818

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