Pattern induction across a homeotic boundary in the wings of Precis coenia (Hbn.) (Lepidoptera: Nymphalidae)

Nijhout, H. Frederik; Rountree, Dorothy B.

doi:10.1016/0020-7322(95)00004-n

Cited by 10 publications

(12 citation statements)

References 14 publications

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“…Our results demonstrate much greater flexibility in the evolutionary response of eyespot sizes compared with color composition, despite the fact that both are characteristics of the same serially repeated color pattern elements on the wings of B. anynana . One explanation for this pattern is that the developmental pathways that regulate production of the focal signal (and determine eyespot size; [ 50 , 51 , 63 ]) are much more flexible and more easily decoupled across a wing surface than the pathways that regulate the threshold level of response to signal concentrations (and determine eyespot color composition; [ 52 , 53 , 64 , 65 ]). Each eyespot-competent area along the wing margin produces its own eyespot organizer [ 51 , 66 ].…”

Section: Resultsmentioning

confidence: 99%

“…Selection targeted pairs of eyespots on two wing surfaces that differ in both morphology and ecological function. Eyespots on the dorsal [ 48 ] and ventral [ 47 ] wing surfaces are thought to function differently in B. anynana ; however, all eyespots are determined by similar spatial and temporal patterns of gene expression [ 63 , 72 ] regardless of their location. This shared development appears to play a primary role in shaping covariation and strongly integrating eyespots among all wing surfaces in Nymphalid butterflies [ 44 , 73 - 76 ], although functional differentiation of some wing characters can also affect patterns of covariation [ 77 ].…”

Section: Resultsmentioning

confidence: 99%

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Differences in the selection response of serially repeated color pattern characters: Standing variation, development, and evolution

et al. 2008

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BackgroundThere is spectacular morphological diversity in nature but lineages typically display a limited range of phenotypes. Because developmental processes generate the phenotypic variation that fuels natural selection, they are a likely source of evolutionary biases, facilitating some changes and limiting others. Although shifts in developmental regulation are associated with morphological differences between taxa, it is unclear how underlying mechanisms affect the rate and direction of evolutionary change within populations under selection.Here we focus on two ecologically relevant features of butterfly wing color patterns, eyespot size and color composition, which are similarly and strongly correlated across the serially repeated eyespots. Though these two characters show similar patterns of standing variation and covariation within a population, they differ in key features of their underlying development. We targeted pairs of eyespots with artificial selection for coordinated (concerted selection) versus independent (antagonistic selection) change in their color composition and size and compared evolutionary responses of the two color pattern characters.ResultsThe two characters respond to selection in strikingly different ways despite initially similar patterns of variation in all directions present in the starting population. Size (determined by local properties of a diffusing inductive signal) evolves flexibly in all selected directions. However, color composition (determined by a tissue-level response to the signal concentration gradient) evolves only in the direction of coordinated change. There was no independent evolutionary change in the color composition of two eyespots in response to antagonistic selection. Moreover, these differences in the directions of short-term evolutionary change in eyespot size and color composition within a single species are consistent with the observed wing pattern diversity in the genus.ConclusionBoth characters respond rapidly to selection for coordinated change, but there are striking differences in their response to selection for antagonistic, independent change across eyespots. While many additional factors may contribute to both short- and long-term evolutionary response, we argue that the compartmentalization of developmental processes can influence the diversification of serial repeats such as butterfly eyespots, even under strong selection.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Differences in the selection response of serially repeated color pattern characters: Standing variation, development, and evolution

et al. 2008

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“…In my laboratory we are working to transform a second butterfly species, Junonia (Precis) coenia , the North American buckeye butterfly, in the family Nymphalidae. This will be useful because J. coenia is already among the most advanced butterfly model systems for understanding lepidopteran color patterns, with numerous gene expression patterns (Carroll et al 1994; Keys et al 1999) and mutants (Nijhout and Rountree 1995; Rountree and Nijhout 1995; Weatherbee et al 1999) already described.…”

Section: Introductionmentioning

confidence: 99%

Jumping genes and AFLP maps: transforming lepidopteran color pattern genetics

Marcus

2005

Evolution and Development

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Summary The color patterns on the wings of lepidopterans are among the most striking patterns in nature and have inspired diverse biological hypotheses such as the ecological role of aposomatic coloration, the evolution of mimicry, the role of human activities in industrial melanism, and the developmental basis of phenotypic plasticity. Yet, the developmental mechanisms underlying color pattern development are not well understood for three reasons. First, few mutations that alter color patterns have been characterized at the molecular level, so there is little mechanistic understanding of how mutant phenotypes are produced. Second, although gene expression patterns resembling adult color patterns are suggestive, there are few data available showing that gene products have a functional role in color pattern formation. Finally, because with few exceptions (notably Bombyx), genetic maps for most species of Lepidoptera are rudimentary or nonexistent, it is very difficult to characterize spontaneous mutants or to determine whether mutations with similar phenotypes are because of lesions in the same gene or different genes. Discussed here are two strategies for overcoming these difficulties: germ‐line transformation of lepidopteran species using transposon vectors and amplified frequency length polymorphism‐based genetic mapping using variation between divergent strains within a species or between closely related and interfertile species. These advances, taken together, will create new opportunities for the characterization of existing genetic variants, the creation of new sequence‐tagged mutants, and the testing of proposed functional genetic relationships between gene products, and will greatly facilitate our understanding of the evolution and development of lepidopteran color patterns.

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“…A total of 19 adult butterflies showed hindwing-to-forewing color pattern transformations, not only replicating the effects of Hindsight on the ventral posterior hindwings but also extending to the dorsal surface and to the anterior compartments ( Supplementary Figures 2-4). Scales of the J. coenia ventral hindwing are normally serrated, contrasting with the rounded shape of their forewing homologs, which allows the delineation of homeotic clones, as in the Hindsight mutants (Nijhout and Rountree, 1995;Weatherbee et al, 1999). For all the pattern elements besides the eyespots, homeotic clones induced a color shift in a cell autonomous fashion, with mutant scale patches showing sharp demarcation from non-mutant scales (Figure 1).…”

Section: Cell-autonomous Homeotic Effects Of Ubx Loss-of-function In mentioning

confidence: 99%

“…In Lepidoptera, two lines of evidence have confirmed the role of Ubx as a homeotic selector gene specifying T3/hindwing identity. A spontaneous mutation called Hindsight, isolated from a Junonia coenia laboratory colony, causes mosaic patches of forewing color pattern and scale identities on the ventral side of butterfly hindwings (Nijhout and Rountree, 1995;Weatherbee et al, 1999). It is unclear if Hindsight is caused by a mutation at the Ubx locus itself, but it induces dominant somatic clones that lack Ubx expression during development, and its restriction to the more posterior region of the T3 appendage is somewhat reminiscent of the Postbithorax and bithoraxoid alleles at the Drosophila Ubx locus, which result in clonal homeotic transformations of the posterior haltere (Adler, 1979(Adler, , 1981.…”

Section: Introductionmentioning

confidence: 99%

Ultrabithorax Is a Micromanager of Hindwing Identity in Butterflies and Moths

et al. 2021

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The forewings and hindwings of butterflies and moths (Lepidoptera) are differentiated from each other, with segment-specific morphologies and color patterns that mediate a wide range of functions in flight, signaling, and protection. The Hox gene Ultrabithorax (Ubx) is a master selector gene that differentiates metathoracic from mesothoracic identities across winged insects, and previous work has shown this role extends to at least some of the color patterns from the butterfly hindwing. Here we used CRISPR targeted mutagenesis to generate Ubx loss-of-function somatic mutations in two nymphalid butterflies (Junonia coenia, Vanessa cardui) and a pyralid moth (Plodia interpunctella). The resulting mosaic clones yielded hindwing-to-forewing transformations, showing Ubx is necessary for specifying many aspects of hindwing-specific identities, including scale morphologies, color patterns, and wing venation and structure. These homeotic phenotypes showed cell-autonomous, sharp transitions between mutant and non-mutant scales, except for clones that encroached into the border ocelli (eyespots) and resulted in composite and non-autonomous effects on eyespot ring determination. In the pyralid moth, homeotic clones converted the folding and depigmented hindwing into rigid and pigmented composites, affected the wing-coupling frenulum, and induced ectopic scent-scales in male androconia. These data confirm Ubx is a master selector of lepidopteran hindwing identity and suggest it acts on many gene regulatory networks involved in wing development and patterning.

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Pattern induction across a homeotic boundary in the wings of Precis coenia (Hbn.) (Lepidoptera: Nymphalidae)

Cited by 10 publications

References 14 publications

Differences in the selection response of serially repeated color pattern characters: Standing variation, development, and evolution

Differences in the selection response of serially repeated color pattern characters: Standing variation, development, and evolution

Jumping genes and AFLP maps: transforming lepidopteran color pattern genetics

Ultrabithorax Is a Micromanager of Hindwing Identity in Butterflies and Moths

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