The genomic basis of colour pattern polymorphism in the harlequin ladybird

Many animal species are comprised of discrete phenotypic forms. Understanding the genetic mechanisms generating and maintaining such phenotypic variation within species is essential to comprehending morphological diversity. A common and conspicuous example of discrete phenotypic variation in natural populations of insects is the occurrence of different colour patterns, which has motivated a rich body of ecological and genetic research1–6. The occurrence of dark, i.e. melanic, forms, displaying discrete colour patterns, is found across multiple taxa, but the underlying genomic basis remains poorly characterized. In numerous ladybird species (Coccinellidae), the spatial arrangement of black and orange patches on adult elytra varies wildly within species, forming strikingly different complex colour patterns7,8. In the harlequin ladybird Harmonia axyridis, more than 200 distinct colour forms have been described, which classic genetic studies suggest result from allelic variation at a single, unknown, locus9,10. Here, we combined whole-genome sequencing, population genomics, gene expression and functional analyses, to establish that the gene pannier controls melanic pattern polymorphism in H. axyridis. We show that pannier, which encodes an evolutionary conserved transcription factor, is necessary for the formation of melanic elements on the elytra. Allelic variation in pannier leads to protein expression in distinct domains on the elytra, and thus determines the distinct colour patterns in H. axyridis. Recombination between pannier alleles may be reduced by a highly divergent sequence of ca. 170 kb in the cis-regulatory regions of pannier with a 50 kb inversion between colour forms. This likely helps maintaining the distinct alleles found in natural populations. Thus we propose that highly variable discrete colour forms can arise in natural populations through cis-regulatory allelic variation of a single gene.

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Phenotypic variation in Heliconius erato crosses shows that iridescent structural colour is sex-linked and controlled by multiple genes

Interface Focus ◽

10.1098/rsfs.2018.0047 ◽

2018 ◽

Vol 9 (1) ◽

pp. 20180047 ◽

Cited By ~ 9

Author(s):

Melanie N. Brien ◽

Juan Enciso-Romero ◽

Andrew J. Parnell ◽

Patricio A. Salazar ◽

Carlos Morochz ◽

...

Keyword(s):

Phenotypic Variation ◽

Genetic Basis ◽

Sex Chromosome ◽

Scattering Data ◽

Colour Pattern ◽

Structural Colour ◽

X Ray Scattering ◽

Multiple Genes ◽

Colour Patterns ◽

Blue Reflectance

Bright, highly reflective iridescent colours can be seen across nature and are produced by the scattering of light from nanostructures. Heliconius butterflies have been widely studied for their diversity and mimicry of wing colour patterns. Despite iridescence evolving multiple times in this genus, little is known about the genetic basis of the colour and the development of the structures which produce it. Heliconius erato can be found across Central and South America, but only races found in western Ecuador and Colombia have developed blue iridescent colour. Here, we use crosses between iridescent and non-iridescent races of H. erato to study phenotypic variation in the resulting F 2 generation. Using measurements of blue colour from photographs, we find that iridescent structural colour is a quantitative trait controlled by multiple genes, with strong evidence for loci on the Z sex chromosome. Iridescence is not linked to the Mendelian colour pattern locus that also segregates in these crosses (controlled by the gene cortex ). Small-angle X-ray scattering data show that spacing between longitudinal ridges on the scales, which affects the intensity of the blue reflectance, also varies quantitatively in F 2 crosses.

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A gynandromorphic grasshopper produced by double fertilization

Australian Journal of Zoology ◽

10.1071/zo9680101 ◽

1968 ◽

Vol 16 (1) ◽

pp. 101 ◽

Cited By ~ 6

Author(s):

MJD White

Keyword(s):

Natural Populations ◽

Colour Pattern ◽

Double Fertilization ◽

Female Side ◽

Zygote Nucleus ◽

Male Side ◽

Pattern Polymorphism ◽

Two Sides

An individual of the large grasshopper Valanga irregularis (Walker) which exhibited bilateral gynandromorphism, is described. The entire right side was female, the left side being male. The colour pattern on the two sides was completely different, the male side corresponding to the concolorous phenotype, the female side to the contrasty one. The gonad was an undeveloped ovotestis, the testicular part being XO (2n = 23). There are two obvious explanations of this gynandromorph: (1) that a single XX zygote nucleus gave rise to XX and XO nuclei through loss of an X; in this case we would be dealing with a sex-linked pattern polymorphism, the gene for the contrasty morph being dominant to the concolorous allele; (2) that the gynandromorph arose from a binucleate egg, as a result of double fertilization. Data on the frequency of the morphs in the two sexes, in natural populations, do not support the first hypothesis, and it is concluded that the second one must be correct.

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A large and diverse autosomal haplotype is associated with sex-linked colour polymorphism in the guppy

10.1101/2021.04.08.437888 ◽

2021 ◽

Author(s):

Josephine R Paris ◽

James R Whiting ◽

Mitchel J Daniel ◽

Joan Ferrer Obiol ◽

Paul J Parsons ◽

...

Keyword(s):

Sexual Selection ◽

Sexual Conflict ◽

Poecilia Reticulata ◽

Sex Chromosome ◽

Colour Polymorphism ◽

Colour Pattern ◽

Whole Genome Sequencing Data ◽

Source Population ◽

Pattern Polymorphism ◽

Colour Patterns

Colour polymorphism provides a tractable trait that can be harnessed to explore the evolution of sexual selection and sexual conflict. Male colour patterns of the Trinidadian guppy (Poecilia reticulata) are governed by both natural and sexual selection, and are typified by extreme pattern colour variation as a result of negative frequency dependent selection. Since guppy colour patterns are often inherited faithfully from fathers to sons, it has been historically presumed that colour genes are physically linked to sex determining loci as a supergene on the sex chromosome. Yet the actual identity and genomic location of the colour pattern genes has remained elusive. We phenotyped and genotyped four guppy Iso-Y lines, where colour was inherited along the patriline, but backcrossed into the stock population every 2 to 3 generations for 40 generations, thereby homogenising the genome at regions unrelated to colour. Using an unbiased phenotyping method to proportion colour pattern differences between and among the Iso-Y lines, we confirmed that the breeding design was successful in producing four distinct colour patterns. Our analysis of genome resequencing data of the four Iso-Y lines uncovered a surprising genetic architecture for colour pattern polymorphism. Genetic differentiation among Iso-Y lines was repeatedly associated with a large and diverse haplotype (~5Mb) on an autosome (LG1), not the sex chromosome (LG12). Moreover, the LG1 haplotype showed elevated linkage disequilibrium and exhibited evidence of sex-specific diversity when we examined whole-genome sequencing data of the natural source population. We hypothesise that colour pattern polymorphism is driven by Y-autosome epistasis, and conclude that predictions of sexual conflict should focus on incorporating the effects of epistasis in understanding complex adaptive architectures.

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Genetic variation in senescence marker protein-30 is associated with natural variation in cold tolerance in Drosophila

Genetics Research ◽

10.1017/s0016672310000108 ◽

2010 ◽

Vol 92 (2) ◽

pp. 103-113 ◽

Cited By ~ 18

Author(s):

KATIE J. CLOWERS ◽

RICHARD F. LYMAN ◽

TRUDY F. C. MACKAY ◽

THEODORE J. MORGAN

Keyword(s):

Cold Tolerance ◽

Phenotypic Variation ◽

Allelic Variation ◽

Balancing Selection ◽

Ion Homeostasis ◽

Natural Populations ◽

Molecular Variation ◽

Marker Protein ◽

Coding Regions ◽

Close Proximity

SummaryA comprehensive understanding of the genetic basis of phenotypic adaptation in nature requires the identification of the functional allelic variation underlying adaptive phenotypes. The manner in which organisms respond to temperature extremes is an adaptation in many species. In the current study, we investigate the role of molecular variation in senescence marker protein-30 (Smp-30) on natural phenotypic variation in cold tolerance in Drosophila melanogaster. Smp-30 encodes a product that is thought to be involved in the regulation of Ca2+ ion homeostasis and has been shown previously to be differentially expressed in response to cold stress. Thus, we sought to assess whether molecular variation in Smp-30 was associated with natural phenotypic variation in cold tolerance in a panel of naturally derived inbred lines from a population in Raleigh, North Carolina. We identified four non-coding polymorphisms that were strongly associated with natural phenotypic variation in cold tolerance. Interestingly, two polymorphisms that were in close proximity to one another (2 bp apart) exhibited opposite phenotypic effects. Consistent with the maintenance of a pair of antagonistically acting polymorphisms, tests of molecular evolution identified a significant excess of maintained variation in this region, suggesting balancing selection is acting to maintain this variation. These results suggest that multiple mutations in non-coding regions can have significant effects on phenotypic variation in adaptive traits within natural populations, and that balancing selection can maintain polymorphisms with opposite effects on phenotypic variation.

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The Genomic Basis of Color Pattern Polymorphism in the Harlequin Ladybird

Current Biology ◽

10.1016/j.cub.2018.08.023 ◽

2018 ◽

Vol 28 (20) ◽

pp. 3296-3302.e7 ◽

Cited By ~ 30

Author(s):

Mathieu Gautier ◽

Junichi Yamaguchi ◽

Julien Foucaud ◽

Anne Loiseau ◽

Aurélien Ausset ◽

...

Keyword(s):

Color Pattern ◽

Harlequin Ladybird ◽

Color Pattern Polymorphism ◽

Pattern Polymorphism ◽

Genomic Basis

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Faculty Opinions recommendation of The genomic basis of color pattern polymorphism in the harlequin ladybird.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.733851514.793552986 ◽

2018 ◽

Author(s):

Yoshinori Tomoyasu

Keyword(s):

Color Pattern ◽

Harlequin Ladybird ◽

Color Pattern Polymorphism ◽

Pattern Polymorphism ◽

Genomic Basis

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The evolution and genetics of sexually dimorphic ‘dual’ mimicry in the butterfly Elymnias hypermnestra

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.2192 ◽

2021 ◽

Vol 288 (1942) ◽

pp. 20202192

Author(s):

Dee M. Ruttenberg ◽

Nicholas W. VanKuren ◽

Sumitha Nallu ◽

Shen-Horn Yen ◽

Djunijanti Peggie ◽

...

Keyword(s):

Sexual Dimorphism ◽

Population Genomics ◽

Model Organism ◽

Single Species ◽

Species Tree ◽

Colour Pattern ◽

Nucleotide Polymorphisms ◽

Wing Colour ◽

Population Structure Analysis ◽

Colour Patterns

Sexual dimorphism is a major component of morphological variation across the tree of life, but the mechanisms underlying phenotypic differences between sexes of a single species are poorly understood. We examined the population genomics and biogeography of the common palmfly Elymnias hypermnestra , a dual mimic in which female wing colour patterns are either dark brown (melanic) or bright orange, mimicking toxic Euploea and Danaus species, respectively. As males always have a melanic wing colour pattern, this makes E. hypermnestra a fascinating model organism in which populations vary in sexual dimorphism. Population structure analysis revealed that there were three genetically distinct E. hypermnestra populations, which we further validated by creating a phylogenomic species tree and inferring historical barriers to gene flow. This species tree demonstrated that multiple lineages with orange females do not form a monophyletic group, and the same is true of clades with melanic females. We identified two single nucleotide polymorphisms (SNPs) near the colour patterning gene WntA that were significantly associated with the female colour pattern polymorphism, suggesting that this gene affects sexual dimorphism. Given WntA 's role in colour patterning across Nymphalidae, E. hypermnestra females demonstrate the repeatability of the evolution of sexual dimorphism.

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HIGH-RESOLUTION CHARACTERIZATION OF MALE ORNAMENTATION AND REEVALUATION OF SEX LINKAGE IN GUPPIES

10.1101/2020.07.14.200329 ◽

2020 ◽

Author(s):

Jake Morris ◽

Iulia Darolti ◽

Wouter van der Bijl ◽

Judith E. Mank

Keyword(s):

High Resolution ◽

Natural Populations ◽

Colour Pattern ◽

Sexually Dimorphic ◽

Animal Colouration ◽

In The Wild ◽

Colour Changes ◽

Colour Patterns ◽

Male Ornaments

AbstractColouration plays a key role in the ecology of many species, influencing how an organism interacts with its environment, other species and conspecifics. Guppies are sexually dimorphic, with males displaying sexually selected colouration resulting from female preference. Previous work has suggested that much of guppy colour pattern variation is Y-linked. However, it remains unclear how many individual colour patterns are Y-linked in natural populations as much of the previous work has focused on phenotypes either not found in the wild, or aggregate measures such as total colour area. Moreover, ornaments have traditionally been identified and delineated by hand, and computational methods now make it possible to extract pixels and identify ornaments more automatedly, reducing the potential for human bias. Here we developed a pipeline for automated ornament identification and high-resolution image analysis of male guppy colour patterns and applied it to a multigenerational pedigree. Our results show that loci controlling the presence or absence of individual male ornaments in our population are not predominantly Y-linked. However, we find that ornaments of similar colour are not independent of each other, and modifier loci that affect whole animal colouration appear to be at least partially Y-linked. Considering these results, Y-linkage of individual ornaments may not be important in driving colour changes in natural populations of guppies, or in expansions of the non-recombining Y region, while Y-linked modifier loci that affect aggregate traits may well play an important role.

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High-resolution characterization of male ornamentation and re-evaluation of sex linkage in guppies

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.1677 ◽

2020 ◽

Vol 287 (1937) ◽

pp. 20201677

Author(s):

Jake Morris ◽

Iulia Darolti ◽

Wouter van der Bijl ◽

Judith E. Mank

Keyword(s):

High Resolution ◽

Natural Populations ◽

Colour Pattern ◽

Sexually Dimorphic ◽

In The Wild ◽

Colour Changes ◽

Colour Patterns ◽

Male Ornaments ◽

Automated Methods

Coloration plays a key role in the ecology of many species, influencing how an organism interacts with its environment, other species and conspecifics. Guppies are sexually dimorphic, with males displaying sexually selected coloration resulting from female preference. Previous work has suggested that much of guppy colour pattern variation is Y-linked. However, it remains unclear how many individual colour patterns are Y-linked in natural populations as much of the previous work has focused on phenotypes either not found in the wild, or aggregate measures such as total colour area. Moreover, ornaments have traditionally been identified and delineated by hand, and computational methods now make it possible to extract pixels and identify ornaments with automated methods, reducing the potential for human bias. Here we developed a pipeline for semi-automated ornament identification and high-resolution image analysis of male guppy colour patterns and applied it to a multigenerational pedigree. Our results show that loci controlling the presence or the absence of individual male ornaments in our population are not predominantly Y-linked. However, we find that ornaments of similar colour are not independent of each other, and modifier loci that affect whole animal coloration appear to be at least partially Y-linked. Considering these results, Y-linkage of individual ornaments may not be important in driving colour changes in natural populations of guppies, or in expansions of the non-recombining Y region, while Y-linked modifier loci that affect aggregate traits may well play an important role.

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