Publications (23)172.43 Total impact
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Article: Multi-Allelic Major Effect Genes Interact with Minor Effect QTLs to Control Adaptive Color Pattern Variation in Heliconius erato.
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ABSTRACT: Recent studies indicate that relatively few genomic regions are repeatedly involved in the evolution of Heliconius butterfly wing patterns. Although this work demonstrates a number of cases where homologous loci underlie both convergent and divergent wing pattern change among different Heliconius species, it is still unclear exactly how many loci underlie pattern variation across the genus. To address this question for Heliconius erato, we created fifteen independent crosses utilizing the four most distinct color pattern races and analyzed color pattern segregation across a total of 1271 F2 and backcross offspring. Additionally, we used the most variable brood, an F2 cross between H. himera and the east Ecuadorian H. erato notabilis, to perform a quantitative genetic analysis of color pattern variation and produce a detailed map of the loci likely involved in the H. erato color pattern radiation. Using AFLP and gene based markers, we show that fewer major genes than previously envisioned control the color pattern variation in H. erato. We describe for the first time the genetic architecture of H. erato wing color pattern by assessing quantitative variation in addition to traditional linkage mapping. In particular, our data suggest three genomic intervals modulate the bulk of the observed variation in color. Furthermore, we also identify several modifier loci of moderate effect size that contribute to the quantitative wing pattern variation. Our results are consistent with the two-step model for the evolution of mimetic wing patterns in Heliconius and support a growing body of empirical data demonstrating the importance of major effect loci in adaptive change.PLoS ONE 01/2013; 8(3):e57033. · 4.09 Impact Factor -
Article: Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand.
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ABSTRACT: Although animals display a rich variety of shapes and patterns, the genetic changes that explain how complex forms arise are still unclear. Here we take advantage of the extensive diversity of Heliconius butterflies to identify a gene that causes adaptive variation of black wing patterns within and between species. Linkage mapping in two species groups, gene-expression analysis in seven species, and pharmacological treatments all indicate that cis-regulatory evolution of the WntA ligand underpins discrete changes in color pattern features across the Heliconius genus. These results illustrate how the direct modulation of morphogen sources can generate a wide array of unique morphologies, thus providing a link between natural genetic variation, pattern formation, and adaptation.Proceedings of the National Academy of Sciences 07/2012; 109(31):12632-7. · 9.68 Impact Factor -
Article: Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation.
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ABSTRACT: Heliconius butterfly wing pattern diversity offers a unique opportunity to investigate how natural genetic variation can drive the evolution of complex adaptive phenotypes. Positional cloning and candidate gene studies have identified a handful of regulatory and pigmentation genes implicated in Heliconius wing pattern variation, but little is known about the greater developmental networks within which these genes interact to pattern a wing. Here we took a large-scale transcriptomic approach to identify the network of genes involved in Heliconius wing pattern development and variation. This included applying over 140 transcriptome microarrays to assay gene expression in dissected wing pattern elements across a range of developmental stages and wing pattern morphs of Heliconius erato. We identified a number of putative early prepattern genes with color-pattern related expression domains. We also identified 51 genes differentially expressed in association with natural color pattern variation. Of these, the previously identified color pattern "switch gene" optix was recovered as the first transcript to show color-specific differential expression. Most differentially expressed genes were transcribed late in pupal development and have roles in cuticle formation or pigment synthesis. These include previously undescribed transporter genes associated with ommochrome pigmentation. Furthermore, we observed upregulation of melanin-repressing genes such as ebony and Dat1 in non-melanic patterns. This study identifies many new genes implicated in butterfly wing pattern development and provides a glimpse into the number and types of genes affected by variation in genes that drive color pattern evolution.BMC Genomics 06/2012; 13:288. · 4.07 Impact Factor -
Article: Butterfly genome reveals promiscuous exchange of mimicry adaptations among species.
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ABSTRACT: The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.Nature 05/2012; · 36.28 Impact Factor -
Article: The benefit of being a social butterfly: communal roosting deters predation.
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ABSTRACT: Aposematic passion-vine butterflies from the genus Heliconius form communal roosts on a nightly basis. This behaviour has been hypothesized to be beneficial in terms of information sharing and/or anti-predator defence. To better understand the adaptive value of communal roosting, we tested these two hypotheses in field studies. The information-sharing hypothesis was addressed by examining following behaviour of butterflies departing from natural roosts. We found no evidence of roost mates following one another to resources, thus providing no support for this hypothesis. The anti-predator defence hypothesis was tested using avian-indiscriminable Heliconius erato models placed singly and in aggregations at field sites. A significantly higher number of predation attempts were observed on solitary models versus aggregations of models. This relationship between aggregation size and attack rate suggests that communally roosting butterflies enjoy the benefits of both overall decreased attack frequency as well as a prey dilution effect. Communal roosts probably deter predators through collective aposematism in which aggregations of conspicuous, unpalatable prey communicate a more effective repel signal to predators. On the basis of our results, we propose that predation by birds is a key selective pressure maintaining Heliconius communal roosting behaviour.Proceedings of the Royal Society B: Biological Sciences 03/2012; 279(1739):2769-76. · 5.41 Impact Factor -
Article: UV photoreceptors and UV-yellow wing pigments in Heliconius butterflies allow a color signal to serve both mimicry and intraspecific communication.
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ABSTRACT: Mimetic wing coloration evolves in butterflies in the context of predator confusion. Unless butterfly eyes have adaptations for discriminating mimetic color variation, mimicry also carries a risk of confusion for the butterflies themselves. Heliconius butterfly eyes, which express recently duplicated ultraviolet (UV) opsins, have such an adaptation. To examine bird and butterfly color vision as sources of selection on butterfly coloration, we studied yellow wing pigmentation in the tribe Heliconiini. We confirmed, using reflectance and mass spectrometry, that only Heliconius use 3-hydroxy-DL-kynurenine (3-OHK), which looks yellow to humans but reflects both UV- and long-wavelength light, whereas butterflies in related genera have chemically unknown yellow pigments mostly lacking UV reflectance. Modeling of these color signals reveals that the two UV photoreceptors of Heliconius are better suited to separating 3-OHK from non-3-OHK spectra compared with the photoreceptors of related genera or birds. The co-occurrence of potentially enhanced UV vision and a UV-reflecting yellow wing pigment could allow unpalatable Heliconius private intraspecific communication in the presence of mimics. Our results are the best available evidence for the correlated evolution of a color signal and color vision. They also suggest that predator visual systems are error prone in the context of mimicry.The American Naturalist 01/2012; 179(1):38-51. · 4.72 Impact Factor -
Article: Wing patterning gene redefines the mimetic history of Heliconius butterflies.
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ABSTRACT: The mimetic butterflies Heliconius erato and Heliconius melpomene have undergone parallel radiations to form a near-identical patchwork of over 20 different wing-pattern races across the Neotropics. Previous molecular phylogenetic work on these radiations has suggested that similar but geographically disjunct color patterns arose multiple times independently in each species. The neutral markers used in these studies, however, can move freely across color pattern boundaries, and therefore might not represent the history of the adaptive traits as accurately as markers linked to color pattern genes. To assess the evolutionary histories across different loci, we compared relationships among races within H. erato and within H. melpomene using a series of unlinked genes, genes linked to color pattern loci, and optix, a gene recently shown to control red color-pattern variation. We found that although unlinked genes partition populations by geographic region, optix had a different history, structuring lineages by red color patterns and supporting a single origin of red-rayed patterns within each species. Genes closely linked (80-250 kb) to optix exhibited only weak associations with color pattern. This study empirically demonstrates the necessity of examining phenotype-determining genomic regions to understand the history of adaptive change in rapidly radiating lineages. With these refined relationships, we resolve a long-standing debate about the origins of the races within each species, supporting the hypothesis that the red-rayed Amazonian pattern evolved recently and expanded, causing disjunctions of more ancestral patterns.Proceedings of the National Academy of Sciences 11/2011; 108(49):19666-71. · 9.68 Impact Factor -
Article: THE ROLE OF ENVIRONMENTAL FACTORS IN THE NORTHEASTERN RANGE EXPANSION OF PAPILIO CRESPHONTES CRAMER (PAPILIONIDAE)
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ABSTRACT: The Giant Swallowtail butterfly, Papilio cresphontes Cramer (Papilionidae), has been reported in New York State for nearly 150 years. In recent years there has been an unexplained increase in P. cresphontes occurrences along the northeastern periphery of its geographi-cal range. This study examined historical records to describe the movement of P. cresphontes populations into New York State and adjacent On-tario. Climate data and field studies were used to identify environmental factors that may influence the range expansion, which was found to cor-respond with an absence of September frosts beginning in 2001. Field studies indicated that some P. cresphontes larvae were capable of withstanding multiple frosts and descended to pupate normally into late October in the range expansion area. Although the larvae may have adapted to endure cooler temperatures to some degree, the effects of warming temperatures on other factors such as natural enemies and lar-val host plant quality in autumn may influence the spread of P. cresphontes populations at least as much as larval frost tolerance. Additional key words: Butterfly range expansion, climate change, biogeography In 1864 the first record of a Giant Swallowtail (Papilio cresphontes Cramer, Papilionidae) was documented for the state of New York (Scudder 1889; Lintner 1893; Comstock & Comstock 1929), but over the last century sightings of this butterfly have been extremely scarce until the past nine years (New York State Butterfly Records 2001–2005; Dirig 2008, 2009). Indeed, over the past decade P. cresphontes has become increasingly abundant in central New York State and appears to be expanding along the northeastern boundary of its range. The causes and characteristics of this recent increase in geographical distribution and population density of P. cresphontes are currently unknown. This paper provides some of the first field data on the presence and survival of P. cresphontes in central New York, and the influence of environmental factors on the range expansion of this butterfly. We followed a P. cresphontes larval field population to pupation, assessing their ability to overwinter in the area and their vulnerability to natural enemies. Weather records were used to examine climatic impacts on larval populations, and literature and historical records revealed distribution and occurrence reports of P. cresphontes. These data suggest that what shapes the geographical distribution of P. cresphontes may not just be host plant abundance, available habitat, or freeze-induced mortality as previously emphasized (Scudder 1889; Wild 1939; Tyler et al. 1994; Hughes 2000; Dennis et al. 2005; Hellman et al. 2008), but may well include the effect of climate on host plant condition and abundance of parasitoids.Journal of the Lepidopterists' Society 08/2011; 65(2):119-125. · 0.27 Impact Factor -
Article: optix drives the repeated convergent evolution of butterfly wing pattern mimicry.
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ABSTRACT: Mimicry--whereby warning signals in different species evolve to look similar--has long served as a paradigm of convergent evolution. Little is known, however, about the genes that underlie the evolution of mimetic phenotypes or to what extent the same or different genes drive such convergence. Here, we characterize one of the major genes responsible for mimetic wing pattern evolution in Heliconius butterflies. Mapping, gene expression, and population genetic work all identify a single gene, optix, that controls extreme red wing pattern variation across multiple species of Heliconius. Our results show that the cis-regulatory evolution of a single transcription factor can repeatedly drive the convergent evolution of complex color patterns in distantly related species, thus blurring the distinction between convergence and homology.Science 07/2011; 333(6046):1137-41. · 31.20 Impact Factor -
Article: Wingless and aristaless2 define a developmental ground plan for moth and butterfly wing pattern evolution.
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ABSTRACT: Butterfly wing patterns have long been a favorite system for studying the evolutionary radiation of complex morphologies. One of the key characteristics of the system is that wing patterns are based on a highly conserved ground plan of pattern homologies. In fact, the evolution of lepidopteran wing patterns is proposed to have occurred through the repeated gain, loss, and modification of only a handful of serially repeated elements. In this study, we examine the evolution and development of stripe wing pattern elements. We show that expression of the developmental morphogen wingless (wg) is associated with early determination of the major basal (B), discal (DI and DII), and marginal (EI) stripe patterns in a broad sampling of Lepidoptera, suggesting homology of these pattern elements across moths and butterflies. We describe for the first time a novel Lepidoptera-specific homeobox gene, aristaless2 (al2), which precedes wg expression during the early determination of DII stripe patterns. We show that al2 was derived from a tandem duplication of the aristaless gene, whereupon it underwent a rapid coding and cis-regulatory divergence relative to its more conserved paralog aristaless1 (al1), which retained an ancestral expression pattern. The al2 stripe expression domain evolutionarily preceded the appearance of the DII pattern elements in multiple lineages, leading us to speculate that al2 represented preexisting positional information that may have facilitated DII evolution via a developmental drive mechanism. In contrast to butterfly eyespot patterns, which are often cited as a key example of developmental co-option of preexisting developmental genes, this study provides an example where the origin of a major color pattern element is associated with the evolution of a novel lepidopteran homeobox gene.Molecular Biology and Evolution 12/2010; 27(12):2864-78. · 5.55 Impact Factor -
Article: Positive selection of a duplicated UV-sensitive visual pigment coincides with wing pigment evolution in Heliconius butterflies.
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ABSTRACT: The butterfly Heliconius erato can see from the UV to the red part of the light spectrum with color vision proven from 440 to 640 nm. Its eye is known to contain three visual pigments, rhodopsins, produced by an 11-cis-3-hydroxyretinal chromophore together with long wavelength (LWRh), blue (BRh) and UV (UVRh1) opsins. We now find that H. erato has a second UV opsin mRNA (UVRh2)-a previously undescribed duplication of this gene among Lepidoptera. To investigate its evolutionary origin, we screened eye cDNAs from 14 butterfly species in the subfamily Heliconiinae and found both copies only among Heliconius. Phylogeny-based tests of selection indicate positive selection of UVRh2 following duplication, and some of the positively selected sites correspond to vertebrate visual pigment spectral tuning residues. Epi-microspectrophotometry reveals two UV-absorbing rhodopsins in the H. erato eye with lambda(max) = 355 nm and 398 nm. Along with the additional UV opsin, Heliconius have also evolved 3-hydroxy-DL-kynurenine (3-OHK)-based yellow wing pigments not found in close relatives. Visual models of how butterflies perceive wing color variation indicate this has resulted in an expansion of the number of distinguishable yellow colors on Heliconius wings. Functional diversification of the UV-sensitive visual pigments may help explain why the yellow wing pigments of Heliconius are so colorful in the UV range compared to the yellow pigments of close relatives lacking the UV opsin duplicate.Proceedings of the National Academy of Sciences 02/2010; 107(8):3628-33. · 9.68 Impact Factor -
Article: Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in Heliconius erato.
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ABSTRACT: Wing pattern evolution in Heliconius butterflies provides some of the most striking examples of adaptation by natural selection. The genes controlling pattern variation are classic examples of Mendelian loci of large effect, where allelic variation causes large and discrete phenotypic changes and is responsible for both convergent and highly divergent wing pattern evolution across the genus. We characterize nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium (LD), and candidate gene expression patterns across two unlinked genomic intervals that control yellow and red wing pattern variation among mimetic forms of Heliconius erato. Despite very strong natural selection on color pattern, we see neither a strong reduction in genetic diversity nor evidence for extended LD across either patterning interval. This observation highlights the extent that recombination can erase the signature of selection in natural populations and is consistent with the hypothesis that either the adaptive radiation or the alleles controlling it are quite old. However, across both patterning intervals we identified SNPs clustered in several coding regions that were strongly associated with color pattern phenotype. Interestingly, coding regions with associated SNPs were widely separated, suggesting that color pattern alleles may be composed of multiple functional sites, conforming to previous descriptions of these loci as "supergenes." Examination of gene expression levels of genes flanking these regions in both H. erato and its co-mimic, H. melpomene, implicate a gene with high sequence similarity to a kinesin as playing a key role in modulating pattern and provides convincing evidence for parallel changes in gene regulation across co-mimetic lineages. The complex genetic architecture at these color pattern loci stands in marked contrast to the single casual mutations often identified in genetic studies of adaptation, but may be more indicative of the type of genetic changes responsible for much of the adaptive variation found in natural populations.PLoS Genetics 01/2010; 6(2):e1000796. · 8.69 Impact Factor -
Article: Genomic hotspots of adaptation in butterfly wing pattern evolution.
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ABSTRACT: What is the genetic architecture of morphological evolution? Is there uniform potential for novelty across a genome or, on the contrary, can a small number of large-effect genes explain the phenotypic variation observed within and between species? Here we highlight recent work on butterfly wing pattern genetics showing that a small set of loci can be repeatedly involved in the evolution of complex traits. These loci behave as genomic hotspots for diversification because they underlie adaptive variation within and between species with both convergent and highly divergent wing patterns. These findings suggest that certain loci may be more likely than others to facilitate rapid evolutionary change.Current opinion in genetics & development 02/2009; 18(6):559-64. · 8.99 Impact Factor -
Article: Gene expression underlying adaptive variation in Heliconius wing patterns: non-modular regulation of overlapping cinnabar and vermilion prepatterns.
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ABSTRACT: Geographical variation in the mimetic wing patterns of the butterfly Heliconius erato is a textbook example of adaptive polymorphism; however, little is known about how this variation is controlled developmentally. Using microarrays and qPCR, we identified and compared expression of candidate genes potentially involved with a red/yellow forewing band polymorphism in H. erato. We found that transcripts encoding the pigment synthesis enzymes cinnabar and vermilion showed pattern- and polymorphism-related expression patterns, respectively. cinnabar expression was associated with the forewing band regardless of pigment colour, providing the first gene expression pattern known to be correlated with a major Heliconius colour pattern. In contrast, vermilion expression changed spatially over time in red-banded butterflies, but was not expressed at detectable levels in yellow-banded butterflies, suggesting that regulation of this gene may be involved with the red/yellow polymorphism. Furthermore, we found that the yellow pigment, 3-hydroxykynurenine, is incorporated into wing scales from the haemolymph rather than being synthesized in situ. We propose that some aspects of Heliconius colour patterns are determined by spatio-temporal overlap of pigment gene transcription prepatterns and speculate that evolutionary changes in vermilion regulation may in part underlie an adaptive colour pattern polymorphism.Proceedings of the Royal Society B: Biological Sciences 02/2008; 275(1630):37-45. · 5.41 Impact Factor -
Article: Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies.
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ABSTRACT: With over 20 parapatric races differing in their warningly colored wing patterns, the butterfly Heliconius erato provides a fascinating example of an adaptive radiation. Together with matching races of its co-mimic Heliconius melpomene, H. erato also represents a textbook case of Müllerian mimicry, a phenomenon where common warning signals are shared amongst noxious organisms. It is of great interest to identify the specific genes that control the mimetic wing patterns of H. erato and H. melpomene. To this end we have undertaken comparative mapping and targeted genomic sequencing in both species. This paper reports on a comparative analysis of genomic sequences linked to color pattern mimicry genes in Heliconius. Scoring AFLP polymorphisms in H. erato broods allowed us to survey loci at approximately 362 kb intervals across the genome. With this strategy we were able to identify markers tightly linked to two color pattern genes: D and Cr, which were then used to screen H. erato BAC libraries in order to identify clones for sequencing. Gene density across 600 kb of BAC sequences appeared relatively low, although the number of predicted open reading frames was typical for an insect. We focused analyses on the D- and Cr-linked H. erato BAC sequences and on the Yb-linked H. melpomene BAC sequence. A comparative analysis between homologous regions of H. erato (Cr-linked BAC) and H. melpomene (Yb-linked BAC) revealed high levels of sequence conservation and microsynteny between the two species. We found that repeated elements constitute 26% and 20% of BAC sequences from H. erato and H. melpomene respectively. The majority of these repetitive sequences appear to be novel, as they showed no significant similarity to any other available insect sequences. We also observed signs of fine scale conservation of gene order between Heliconius and the moth Bombyx mori, suggesting that lepidopteran genome architecture may be conserved over very long evolutionary time scales. Here we have demonstrated the tractability of progressing from a genetic linkage map to genomic sequence data in Heliconius butterflies. We have also shown that fine-scale gene order is highly conserved between distantly related Heliconius species, and also between Heliconius and B. mori. Together, these findings suggest that genome structure in macrolepidoptera might be very conserved, and show that mapping and positional cloning efforts in different lepidopteran species can be reciprocally informative.BMC Genomics 01/2008; 9:345. · 4.07 Impact Factor -
Article: Localization of Müllerian mimicry genes on a dense linkage map of Heliconius erato.
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ABSTRACT: We report a dense genetic linkage map of Heliconius erato, a neotropical butterfly that has undergone a remarkable adaptive radiation in warningly colored mimetic wing patterns. Our study exploited natural variation segregating in a cross between H. erato etylus and H. himera to localize wing color pattern loci on a dense linkage map containing amplified fragment length polymorphisms (AFLP), microsatellites, and single-copy nuclear loci. We unambiguously identified all 20 autosomal linkage groups and the sex chromosome (Z). The map spanned a total of 1430 Haldane cM and linkage groups varied in size from 26.3 to 97.8 cM. The average distance between markers was 5.1 cM. Within this framework, we localized two major color pattern loci to narrow regions of the genome. The first gene, D, responsible for red/orange elements, had a most likely placement in a 6.7-cM region flanked by two AFLP markers on the end of a large 87.5-cM linkage group. The second locus, Sd, affects the melanic pattern on the forewing and was found within a 6.3-cM interval between flanking AFLP loci. This study complements recent linkage analysis of H. erato's comimic, H. melpomene, and forms the basis for marker-assisted physical mapping and for studies into the comparative genetic architecture of wing-pattern mimicry in Heliconius.Genetics 07/2006; 173(2):735-57. · 4.01 Impact Factor -
Article: Wing venation and Distal-less expression in Heliconius butterfly wing pattern development.
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ABSTRACT: Here we show that major color pattern elements of Heliconius butterfly wings develop independently of wing venation. We recovered a hybrid Heliconius displaying a mutant phenotype with a severe vein deficiency. Although this butterfly lacked most of its wing veins, the large, melanic banding patterns typical of the genus were conserved across the entire wing. The only obvious correlation between vein reduction and pigment patterns was a loss of vein-associated melanin stripes near the distal margin of the wings. We examined the expression of the eyespot-associated transcription factor Distal-less in a banded and a spotted species of Heliconius and found no obvious relationship between protein expression and the band or spot patterns typical of the genus. Together, our results suggest that the melanic bands and spots in Heliconius are unlikely to be derived from an eyespot determination system. We propose that major elements of Heliconius wing pattern formation are based primarily on a complex, whole-wing proximodistal axis system.Archiv für Entwickelungsmechanik der Organismen 01/2005; 214(12):628-34. · 1.77 Impact Factor -
Article: Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process.
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ABSTRACT: In butterflies there is a class of "intervein" wing patterns that have lines of symmetry halfway between wing veins. These patterns occur in a range of shapes, including eyespots, ellipses, and midlines, and were proposed to have evolved through developmental shifts along a midline-to-eyespot continuum. Here we show that Notch (N) upregulation, followed by activation of the transcription factor Distal-less (Dll), is an early event in the development of eyespot and intervein midline patterns across multiple species of butterflies. A relationship between eyespot phenotype and N and Dll expression is demonstrated in a loss-of-eyespot mutant in which N and Dll expression is reduced at missing eyespot sites. A phylogenetic comparison of expression time series from eight moth and butterfly species suggests that intervein N and Dll patterns are a derived characteristic of the butterfly lineage. Furthermore, prior to eyespot determination in eyespot-bearing butterflies, N and Dll are transiently expressed in a pattern that resembles ancestral intervein midline patterns. In this study we establish N upregulation as the earliest known event in eyespot determination, demonstrate gene expression associated with intervein midline color patterns, and provide molecular evidence that wing patterns evolved through addition to and truncation of a conserved midline-to-eyespot pattern formation sequence.Current Biology 08/2004; 14(13):1159-66. · 9.65 Impact Factor -
Article: Evidence for Notch-mediated lateral inhibition in organizing butterfly wing scales.
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ABSTRACT: Here I present gene expression data that implicate a Notch-mediated lateral inhibition process in the spatial organization of butterfly wing scales. During early pupal development the receptor molecule Notch is expressed in a grid-like pattern in the wing epithelium, resulting in parallel rows of uniformly spaced cells with low Notch expression. Previous work has shown that these low-Notch cells express a homolog of the achaete-scute proneural transcription factors and develop into scales. All of these observations are consistent with the Drosophila model of Notch-mediated bristle determination and support the hypothesis that bristles and scales share an underlying patterning mechanism.Archiv für Entwickelungsmechanik der Organismen 02/2004; 214(1):43-6. · 1.77 Impact Factor -
Article: Evolutionary redeployment of a biosynthetic module: expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development.
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ABSTRACT: Ommochromes are common among insects as visual pigments; however, in some insect lineages ommochromes have evolved novel functions such as integument coloration and tryptophan secretion. One role of ommochromes, as butterfly wing pigments, can apparently be traced to a single origin in the family Nymphalidae. The synthesis and storage of ommochrome pigments is a complex process that requires the concerted activity of multiple enzyme and transporter molecules. To help understand how this subcellular process appeared in a novel context during evolution, we explored aspects of ommochrome pigment development in the wings of the nymphalid butterfly Vanessa cardui. Using chromatography and radiolabeled precursor incorporation studies we identified the ommochrome xanthommatin as a V. cardui wing pigment. We cloned fragments of two ommochrome enzyme genes, vermilion and cinnabar, and an ommochrome precursor transporter gene, white, and found that these genes were transcribed in wing tissue at relatively high levels during wing scale development. Unexpectedly, however, the spatial patterns of transcription were not associated in a simple way with adult pigment patterns. Although our results suggest that the evolution of ommochrome synthesis in butterfly wings likely arose in part through novel regulation of vermilion, cinnabar, and white transcription, they also point to a complex relationship between transcriptional prepatterns and pigment synthesis in V. cardui.Evolution & Development 7(4):301-11. · 2.47 Impact Factor
Top co-authors
Top Journals
Institutions
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2006–2013
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University of Puerto Rico at Rio Piedras
- • Center for Applied Tropical Ecology and Conservation (CREST-CATEC)
- • Department of Biology
San Juan, San Juan, Puerto Rico
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2010–2012
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North Carolina State University
- Department of Genetics
Raleigh, NC, USA
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2008–2012
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University of California, Irvine
- Department of Ecology and Evolutionary Biology
Irvine, CA, USA
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2005
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Duke University
- Department of Biology
Durham, NC, USA
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2004
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The University of Arizona
- Department of Molecular and Cellular Biology
Tucson, AZ, USA
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