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Robert D Reed

Publications and source records attributed to Robert D Reed.

6 recordsLinked to original sources

Localization of Müllerian mimicry genes on a dense linkage map of Heliconius erato.

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.

Adaptation, Physiological↗

Wing venation and Distal-less expression in Heliconius butterfly wing pattern development.

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.

Animals↗

Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process.

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.

Animals↗

Evidence for Notch-mediated lateral inhibition in organizing butterfly wing scales.

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.

Animals↗

Evolutionary redeployment of a biosynthetic module: expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development.

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.

Amino Acid Sequence↗

Cryptic variation in butterfly eyespot development: the importance of sample size in gene expression studies.

Previous studies have shown that development can be robust to variation in parameters such as the timing or level of gene expression. This leads to the prediction that natural populations should be able to host developmental variation that has little phenotypic effect. Cryptic variation is of particular interest because it can result in selectable phenotypes when "released" by environmental or genetic factors. Currently, however, we have little idea of how variation is distributed between genes or over time in pattern formation processes. Here we survey expression of Notch (N), Spalt (Sal), and Engrailed (En) during butterfly eyespot determination to better understand how pattern formation may vary within a population. We observed substantial heterochronic variance in the progress of spatial expression patterns for all three proteins, suggesting some degree of developmental buffering in eyespot development. Peak variance for different proteins was found at both early and late stages of development, contrasting with previous models suggesting that the distribution of variance should be more temporally focused during pattern formation. We speculate that our observations are representative of a standing reservoir of cryptic variation that may contribute to phenotypic evolution under certain circumstances. Our results also provide a strong cautionary message that gene expression studies with limited sample sizes can be positively misleading in terms of inferring expression pattern time series, as well as for making cross-species phylogenetic comparisons.

Animals↗