scholarly journals Genetic Basis of Melanin Pigmentation in Butterfly Wings

2017 ◽  
Author(s):  
Linlin Zhang ◽  
Arnaud Martin ◽  
Michael W. Perry ◽  
Karin R.L. van der Burg ◽  
Yuji Matsuoka ◽  
...  

AbstractDespite the variety, prominence, and adaptive significance of butterfly wing patterns surprisingly little known about the genetic basis of wing color diversity. Even though there is intense interest in wing pattern evolution and development, the technical challenge of genetically manipulating butterflies has slowed efforts to functionally characterize color pattern development genes. To identify candidate wing pigmentation genes we used RNA-seq to characterize transcription across multiple stages of butterfly wing development, and between different color pattern elements, in the painted lady butterfly Vanessa cardui. This allowed us to pinpoint genes specifically associated with red and black pigment patterns. To test the functions of a subset of genes associated with presumptive melanin pigmentation we used CRISPR/Cas9 genome editing in four different butterfly genera. pale, Ddc, and yellow knockouts displayed reduction of melanin pigmentation, consistent with previous findings in other insects. Interestingly, however, yellow-d, ebony, and black knockouts revealed that these genes have localized effects on tuning the color of red, brown, and ochre pattern elements. These results point to previously undescribed mechanisms for modulating the color of specific wing pattern elements in butterflies, and provide an expanded portrait of the insect melanin pathway.

2017 ◽  
Vol 114 (40) ◽  
pp. 10707-10712 ◽  
Author(s):  
Linlin Zhang ◽  
Anyi Mazo-Vargas ◽  
Robert D. Reed

The optix gene has been implicated in butterfly wing pattern adaptation by genetic association, mapping, and expression studies. The actual developmental function of this gene has remained unclear, however. Here we used CRISPR/Cas9 genome editing to show that optix plays a fundamental role in nymphalid butterfly wing pattern development, where it is required for determination of all chromatic coloration. optix knockouts in four species show complete replacement of color pigments with melanins, with corresponding changes in pigment-related gene expression, resulting in black and gray butterflies. We also show that optix simultaneously acts as a switch gene for blue structural iridescence in some butterflies, demonstrating simple regulatory coordination of structural and pigmentary coloration. Remarkably, these optix knockouts phenocopy the recurring “black and blue” wing pattern archetype that has arisen on many independent occasions in butterflies. Here we demonstrate a simple genetic basis for structural coloration, and show that optix plays a deeply conserved role in butterfly wing pattern development.


2019 ◽  
Vol 36 (12) ◽  
pp. 2842-2853 ◽  
Author(s):  
Nicholas W VanKuren ◽  
Darli Massardo ◽  
Sumitha Nallu ◽  
Marcus R Kronforst

Abstract Some genes have repeatedly been found to control diverse adaptations in a wide variety of organisms. Such gene reuse reveals not only the diversity of phenotypes these unique genes control but also the composition of developmental gene networks and the genetic routes available to and taken by organisms during adaptation. However, the causes of gene reuse remain unclear. A small number of large-effect Mendelian loci control a huge diversity of mimetic butterfly wing color patterns, but reasons for their reuse are difficult to identify because the genetic basis of mimicry has primarily been studied in two systems with correlated factors: female-limited Batesian mimicry in Papilio swallowtails (Papilionidae) and non-sex-limited Müllerian mimicry in Heliconius longwings (Nymphalidae). Here, we break the correlation between phylogenetic relationship and sex-limited mimicry by identifying loci controlling female-limited mimicry polymorphism Hypolimnas misippus (Nymphalidae) and non-sex-limited mimicry polymorphism in Papilio clytia (Papilionidae). The Papilio clytia polymorphism is controlled by the genome region containing the gene cortex, the classic P supergene in Heliconius numata, and loci controlling color pattern variation across Lepidoptera. In contrast, female-limited mimicry polymorphism in Hypolimnas misippus is associated with a locus not previously implicated in color patterning. Thus, although many species repeatedly converged on cortex and its neighboring genes over 120 My of evolution of diverse color patterns, female-limited mimicry polymorphisms each evolved using a different gene. Our results support conclusions that gene reuse occurs mainly within ∼10 My and highlight the puzzling diversity of genes controlling seemingly complex female-limited mimicry polymorphisms.


2018 ◽  
Author(s):  
Richard M. Merrill ◽  
Pasi Rastas ◽  
Maria C. Melo ◽  
Sarah Barker ◽  
John Davey ◽  
...  

AbstractThe evolution of new species is made easier when traits under divergent ecological selection are also mating cues. Such ecological mating cues are now considered more common than previously thought, but we still know little about the genetic changes underlying their evolution, or more generally about the genetic basis for assortative mating behaviors. The warning patterns of Heliconius melpomene and H. cydno are under disruptive selection due to increased predation of non-mimetic hybrids, and are used during mate recognition. We carried out a genome-wide quantitative trait locus (QTL) analysis of preference behaviors between these species and showed that divergent male preference has a simple genetic basis. Three QTLs each explain a large proportion of the differences in preference behavior observed between the parental species. Two of these QTLs are on chromosomes with major color pattern genes, including one that is tightly associated with the gene optix. Different loci influence different aspects of attraction, suggesting that behavioral isolation in Heliconius involves the evolution of independently segregating modules, similar to those for the corresponding wing pattern cues. Hybridization and subsequent sharing of wing pattern loci has played an important role during adaptation and speciation in Heliconius butterflies. The existence of large effect preference loci could similarly assist the evolution of novel behavioral phenotypes through recombination and introgression, and should facilitate rapid speciation.


Development ◽  
1994 ◽  
Vol 1994 (Supplement) ◽  
pp. 225-233
Author(s):  
H. Frederik Nijhout

The wing patterns of butterflies are made up of an array of discrete pattern elements. Wing patterns evolve through changes in the size, shape and color of these pattern elements. The pattern elements are arranged in several parallel symmetry systems that develop independently from one another. The wing is further compartmentalized for color pattern formation by the wing veins. Pattern development in these compartments is largely independent from that in adjacent compartments. This two-fold compartmentalization of the color pattern (by symmetry systems and wing veins) has resulted in an extremely flexible developmental system that allows each pattern element to vary and evolve independently, without the burden of correlated evolution in other elements. The lack of developmental constraints on pattern evolution may explain why butterflies have diverged so dramatically in their color patterns, and why accurate mimicry has evolved so frequently. This flexible developmental system appears to have evolved from the convergence of two ancient patterning systems that the butterflies inherited from their ancestors. Mapping of various pattern types onto a phylogeny of the Lepidoptera indicates that symmetry systems evolved in several steps from simple spotting patterns. Initially all such patterns were developmentally identical but each became individuated in the immediate ancestors of the butterflies. Compartmentalization by wing veins is found in all Lepidoptera and their sister group the Trichoptera, but affects primarily the ripple patterns that form the background upon which spotting patterns and symmetry systems develop. These background pattern are determined earlier in ontogeny than are the symmetry systems, and the compartmentalization mechanism is presumably no longer active when the latter develop. It appears that both individuation of symmetry systems and compartmentalization by the wing veins began at or near the wing margin. Only the butterflies and their immediate ancestors evolved a pattern formation mechanism that combines the development of a regular array of well-differentiated symmetry systems with the mechanism that compartmentalizes the wing with respect to color pattern formation. The result was an uncoupling of symmetry system development in each wing cell. This, together with the individuation of symmetry systems, yielded an essentially mosaic developmental system of unprecedented permutational flexibility that enabled the great radiation of butterfly wing patterns.


2020 ◽  
Author(s):  
V Llaurens ◽  
Y Le Poul ◽  
A Puissant ◽  
C Noûs ◽  
P Blandin ◽  
...  

AbstractSpecies interactions such as mimicry can promote trait convergence but disentangling this effect from those of shared ecology, evolutionary history and niche conservatism is often challenging. Here by focusing on wing color pattern variation within and between three butterfly species living in sympatry in a large proportion of their range, we tested the effect of species interactions on trait diversification. These butterflies display a conspicuous iridescent blue coloration on the dorsal side of their wings and a cryptic brownish colour on the ventral side. Combined with an erratic and fast flight, these color patterns increase the difficulty of capture by predators and contribute to the high escape abilities of these butterflies. We hypothesize that, beyond their direct contribution to predator escape, these wing patterns can be used as signals of escape abilities by predators, resulting in positive frequency-dependent selection favouring convergence in wing pattern in sympatry. To test this hypothesis, we quantified dorsal wing pattern variations of 723 butterflies from the three species sampled throughout their distribution, including sympatric and allopatric situations and compared the phenotypic distances between species, sex and localities. We detected a significant effect of localities on colour pattern, and higher inter-specific resemblance in sympatry as compared to allopatry, consistent with the hypothesis of local convergence of wing patterns. Our results provide some support to the existence of escape mimicry in the wild and stress the importance of estimating trait variation within species to understand trait variation between species, and to a larger extent, trait diversification at the macro-evolutionary scale.


PeerJ ◽  
2020 ◽  
Vol 8 ◽  
pp. e8263
Author(s):  
Sandra R. Schachat

The nymphalid groundplan, an idealized schematic illustrating the essential elements of butterfly wing patterns, predicts a consistent relationship between color pattern and wing venation. Moths in the family Geometridae have wing shapes and patterns that often resemble those of butterflies, and until recently, this family was believed to be among butterflies’ closest relatives. However, an examination of the geometrid genus Dichromodes Guenée, 1858 shows no consistent relationship between the central symmetry system and wing venation. Whereas the distal edge of the central symmetry system is predicted to reach the costal margin proximal to the Subcostal vein in butterflies and acronictine moths, it has no consistent relationship with the Subcostal, Radius, or Radial Sector 1 veins in Dichromodes. This finding highlights developmental diversity that was previously overlooked due to the overwhelming preference for butterflies in studies of lepidopteran wing patterns.


2017 ◽  
Vol 114 (40) ◽  
pp. 10701-10706 ◽  
Author(s):  
Anyi Mazo-Vargas ◽  
Carolina Concha ◽  
Luca Livraghi ◽  
Darli Massardo ◽  
Richard W. R. Wallbank ◽  
...  

Butterfly wing patterns provide a rich comparative framework to study how morphological complexity develops and evolves. Here we used CRISPR/Cas9 somatic mutagenesis to test a patterning role for WntA, a signaling ligand gene previously identified as a hotspot of shape-tuning alleles involved in wing mimicry. We show that WntA loss-of-function causes multiple modifications of pattern elements in seven nymphalid butterfly species. In three butterflies with a conserved wing-pattern arrangement, WntA is necessary for the induction of stripe-like patterns known as symmetry systems and acquired a novel eyespot activator role specific to Vanessa forewings. In two Heliconius species, WntA specifies the boundaries between melanic fields and the light-color patterns that they contour. In the passionvine butterfly Agraulis, WntA removal shows opposite effects on adjacent pattern elements, revealing a dual role across the wing field. Finally, WntA acquired a divergent role in the patterning of interveinous patterns in the monarch, a basal nymphalid butterfly that lacks stripe-like symmetry systems. These results identify WntA as an instructive signal for the prepatterning of a biological system of exuberant diversity and illustrate how shifts in the deployment and effects of a single developmental gene underlie morphological change.


Sign in / Sign up

Export Citation Format

Share Document