The Developmental Role of Agouti in Color Pattern Evolution

A regulatory mutation affecting expression of the Agouti gene shows color-specific selection in beach mice. Animal color patterns can affect fitness in the wild; however, little is known about the mechanisms that control their formation and subsequent evolution. We took advantage of two locally camouflaged populations of Peromyscus mice to show that the negative regulator of adult pigmentation, Agouti, also plays a key developmental role in color pattern evolution. Genetic and functional analyses showed that ventral-specific embryonic expression of Agouti establishes a prepattern by delaying the terminal differentiation of ventral melanocytes. Moreover, a skin-specific increase in both the level and spatial domain of Agouti expression prevents melanocyte maturation in a regionalized manner, resulting in a novel and adaptive color pattern. Thus, natural selection favors late-acting, tissue-specific changes in embryonic Agouti expression to produce large changes in adult color pattern.

• Publication year

  2011

• Venue

  Science

• Publication date

  2011-02-25

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1126/science.1200684PMID 21350176
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Convergence in pigmentation at multiple levels: mutations, genes and function

  2010cited by this paper
• THE SELECTIVE ADVANTAGE OF CRYPSIS IN MICE

  2010cited by this paper
• Not just black and white: pigment pattern development and evolution in vertebrates.

  2009cited by this paper
• Microarray analysis sheds light on the dedifferentiating role of agouti signal protein in murine melanocytes via the Mc1r

  2009cited by this paper
• Is Genetic Evolution Predictable?

  2009cited by this paper
• Melanism in Peromyscus Is Caused by Independent Mutations in Agouti

  2009cited by this paper
• Metamodels and Phylogenetic Replication: A Systematic Approach to the Evolution of Developmental Pathways

  2009cited by this paper
• Ultrasound-guided in utero injections allow studies of the development and function of the eye

  2008cited by this paper
• Evo‐Devo and an Expanding Evolutionary Synthesis

  2008cited by this paper
• Natural Selection Along an Environmental Gradient: A Classic Cline in Mouse Pigmentation

  2008cited by this paper
• Adaptive Variation in Beach Mice Produced by Two Interacting Pigmentation Genes

  2007cited by this paper
• Archaeology in Northeast Asia : on the pathway to Bering Strait

  2006cited by this paper
• The First Americans: Race, Evolution, and the Origin of Native Americans. By Joseph F Powell. Cambridge and New York: Cambridge University Press. $110.00 (hardcover); $35.00 (paper). viii + 268 p; ill.; index. ISBN: 0–521–82350–1 (hc); 0–521–53035–0 (pb). 2005.

  2006cited by this paper
• Ice Age people of North America : environments, origins, and adaptations

  2005cited by this paper
• IL-13受体α2降低血吸虫病肉芽肿的炎症反应并延长宿主存活时间[英]/Mentink-Kane MM,Cheever AW，Thompson RW，et al//Proc Natl Acad Sci U S A

  2005cited by this paper
• Dorsoventral Patterning of the Mouse Coat by Tbx15

  2004cited by this paper
• Fate of melanocytes during development of the hair follicle pigmentary unit.

  2003cited by this paper
• Pigment patterns: fish in stripes and spots.

  2003cited by this paper
• How the zebrafish gets its stripes.

  2001cited by this paper
• Effects of genic substitution at the agouti, brown, albino, dilute, and pink-eyed dilution loci on the proliferation and differentiation of mouse epidermal melanocytes in serum-free culture.

  1998cited by this paper
• American beginnings. the prehistory and palaeoecology of Beringia

  1998cited by this paper
• Modulation of murine melanocyte function in vitro by agouti signal protein

  1997cited by this paper
• Evolution

  1996cited by this paper
• The genetics of pigmentation: from fancy genes to complex traits.

  1996cited by this paper
• Opposite orientations of an inverted duplication and allelic variation at the mouse agouti locus.

  1996cited by this paper
• Development

  1996cited by this paper
• Expression and transgenic studies of the mouse agouti gene provide insight into the mechanisms by which mammalian coat color patterns are generated.

  1995cited by this paper
• Molecular analysis of reverse mutations from nonagouti (a) to black-and-tan (a(t)) and white-bellied agouti (Aw) reveals alternative forms of agouti transcripts.

  1994cited by this paper
• Molecular and developmental genetics of mouse coat color.

  1994cited by this paper
• Differences in dorsal and ventral pigmentation result from regional expression of the mouse agouti gene.

  1994cited by this paper
• The agouti gene: turned on to yellow.

  1994cited by this paper
• Molecular characterization of the mouse agouti locus.

  1992cited by this paper
• The development and evolution of butterfly wing patterns

  1991cited by this paper
• Genetics

  1981cited by this paper
• Geoarchaeology

  1979cited by this paper
• Adaptive Coloration in Animals

  1940cited by this paper

• Genomic basis of the evolution of vertical bars in clownfishes

  2026cites this paper
• PMEL governs autosomal dominant inheritance of white-tail independent of yellow body plumage in chickens (Gallus gallus domesticus)

  2025cites this paper
• Drosophila melanogaster pigmentation demonstrates adaptive phenotypic parallelism over multiple spatiotemporal scales

  2025cites this paper
• A physiological and histological atlas of reproduction in the North American deer mouse (Peromyscus maniculatus)

  2025cites this paper
• Unmasking cryptic mice: the dominant role of ventral pelage colour in distinguishing syntopic Apodemus (A. sylvaticus-A. flavicollis)

  2025cites this paper
• Agouti and BMP signaling drive a naturally occurring fate conversion of melanophores to leucophores in zebrafish

  2025cites this paper
• White eye-rings coevolved with diurnal behaviors as a trait enhancing visual appeal in rodents

  2025cites this paper
• Contributions of epigenomic and epitranscriptomic methylation to animal colouration.

  2025cites this paper
• Unveiling cell-type-specific mode of evolution in comparative single-cell expression data.

  2025cites this paper
• Disruption of mc1r Disturbs Skin Pigmentation in Xenopus tropicalis

  2025cites this paper
• Transcriptome Analysis of Natural Albino Northern Snakehead (Channa argus var.) Provides Novel Insights into Color-Related Genes

  2025cites this paper
• Comparative transcriptome and methylome of polar bears, giant and red pandas reveal diet‐driven adaptive evolution

  2024cites this paper
• Structure, function and formation of the amniote skin pattern.

  2024cites this paper
• The period gene alters daily and seasonal timing in Ostrinia nubilalis

  2024cites this paper
• Genomic analysis reveals the association of KIT and MITF variants with the white spotting in swamp buffaloes

  2024cites this paper
• col1a2+ fibroblasts/muscle progenitors finetune xanthophore countershading by differentially expressing csf1a/1b in embryonic zebrafish

  2024cites this paper
• Genetic mechanisms of animal camouflage: an interdisciplinary perspective.

  2024cites this paper
• Exposure to sulfur in soil explains pigmentation by pheomelanin in birds inhabiting Iceland

  2023cites this paper
• Two novel, tightly linked, and rapidly evolving genes underlie Aedes aegypti mosquito reproductive resilience during drought

  2023cites this paper
• Analysis of the genetic loci of pigment pattern evolution in vertebrates

  2023cites this paper
• Transcriptome analyses of betta fish (Betta splendens) provide novel insights into fin regeneration and color-related genes.

  2023cites this paper
• Mechanisms Underlying the Formation and Evolution of Vertebrate Color Patterns.

  2023cites this paper
• The effects of mutations on gene expression and alternative splicing: a case study of EMS-induced heritable mutations in the microcrustacean Daphnia

  2023cites this paper
• Development shapes the evolutionary diversification of rodent stripe patterns

  2023cites this paper
• The evolution of white-tailed jackrabbit camouflage in response to past and future seasonal climates

  2023cites this paper
• Ecological Speciation Promoted by Divergent Regulation of Functional Genes Within African Cichlid Fishes

  2022cites this paper
• Additive genetic effects in interacting species jointly determine the outcome of caterpillar herbivory

  2022cites this paper
• Role of the melanocortin system in zebrafish skin physiology.

  2022cites this paper
• Functional divergence of the pigmentation gene melanocortin-1 receptor (MC1R) in six endemic Macaca species on Sulawesi Island

  2022cites this paper
• Neural crest cells as a source of microevolutionary variation

  2022cites this paper
• Corin: A Key Mediator in Sodium Homeostasis, Vascular Remodeling, and Heart Failure

  2022cites this paper
• Chromatin activity identifies differential gene regulation across human ancestries

  2022cites this paper
• A conserved molecular template underlies color pattern diversity in estrildid finches

  2022cites this paper
• An enhancer of Agouti contributes to parallel evolution of cryptically colored beach mice

  2021influential citation
• A novel fish behavior: “floating” of Paramisgurnus dabryanus loaches

  2021cites this paper
• Functional conservation and divergence of color-pattern-related agouti family genes in teleost fishes.

  2021cites this paper
• Adaptive tail-length evolution in deer mice is associated with differential Hoxd13 expression in early development

  2021cites this paper
• Unraveling patterns of disrupted gene expression across a complex tissue

  2021cites this paper
• Museomics Dissects the Genetic Basis for Adaptive Seasonal Coloration in the Least Weasel

  2021cites this paper
• A Common Endocrine Signature Marks the Convergent Evolution of an Elaborate Dance Display in Frogs

  2021cites this paper
• Evolution of Pigment Pattern Formation in Teleosts

  2021cites this paper
• Parallel evolution of apetalous lineages within the buttercup family (Ranunculaceae): Outward expansion of AGAMOUS1, rather than disruption of APETALA3-3.

  2020cites this paper
• Mechanisms of Change: A Population-Based Perspective on the Roles of Modularity and Pleiotropy in Diversification

  2020cites this paper
• The embryonic origin of periodic color patterns.

  2020cites this paper
• Skin transcriptome profiles associated with black- and white-coated regions in Boer and Macheng black crossbred goats.

  2020cites this paper
• Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus

  2020cites this paper
• Transcriptomic regulation of seasonal coat color change in hares

  2020cites this paper
• Genetic deciphering of the antagonistic activities of the melanin-concentrating hormone and melanocortin pathways in skin pigmentation

  2020cites this paper
• Ecological divergence in sympatry causes gene misexpression in hybrids

  2020cites this paper
• Different Sources of Allelic Variation Drove Repeated Color Pattern Divergence in Cichlid Fishes

  2020cites this paper
• Genomic Analysis Revealed a Convergent Evolution of LINE-1 in Coat Color: A Case Study in Water Buffaloes (Bubalus bubalis)

  2020cites this paper
• [The embryonic origin of periodic colour patterns].

  2020cites this paper
• The embryonic origin of periodic colour patterns

  2020cites this paper
• Coloration in Mammals.

  2020cites this paper
• Avian Pigment Pattern Formation: Developmental Control of Macro- (Across the Body) and Micro- (Within a Feather) Level of Pigment Patterns

  2020cites this paper
• Developmental bias, macroevolution, and the fossil record

  2019cites this paper
• A simple genetic architecture and low constraint allows rapid floral evolution in a diverse and recently radiating plant genus

  2019cites this paper
• The role of genomic vs. epigenomic variation in shaping patterns of convergent transcriptomic variation across continents in a young species complex

  2019cites this paper
• Molecular Characterization of Species of the Subgenus Mus from Myanmar.

  2019cites this paper
• Molecular mechanisms of convergent color pattern evolution.

  2019cites this paper
• Ecological divergence in sympatry causes gene misregulation in hybrids

  2019cites this paper
• Periodic patterns in Rodentia: Development and evolution

  2019cites this paper
• Regulation of melanocyte stem cells in the pigmentation of skin and its appendages: Biological patterning and therapeutic potentials

  2019cites this paper
• ADAPTIVE POTENTIAL TO CAMOUFLAGE MISMATCH: PLASTIC AND EVOLUTIONARY RESPONSES TO A CLIMATE CHANGE STRESSOR

  2019cites this paper
• Characterization and expression analysis of KIT and MITF‐M genes in llamas and their relation to white coat color

  2019cites this paper
• The adaptive potential of the M-domain of yeast Hsp90

  2019cites this paper
• Comparative Genomics Reveals Accelerated Evolution of Fright Reaction Genes in Ostariophysan Fishes

  2019cites this paper
• Evolution of DNA Methylation in Papio Baboons

  2019cites this paper
• Cloudy with a Chance of Insights: Context Dependent Gene Regulation and Implications for the Evolution of Gene Expression

  2019cites this paper
• Integrated analysis of long non-coding RNA and mRNA expression in different colored skin of koi carp

  2019cites this paper
• Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range

  2019cites this paper
• Screening and analysis of agouti signaling protein interaction partners in Pelodiscus sinensis suggests a role in lipid metabolism.

  2019cites this paper
• Génomique de la spéciation chez le Grand Corégone (Coregonus clupeaformis) : caractérisation des bases génomiques associées à la différenciation phénotypique

  2019cites this paper
• Bar, stripe and spot development in sand-dwelling cichlids from Lake Malawi

  2019cites this paper
• Instructive role of melanocytes during pigment pattern formation of the avian skin

  2019cites this paper
• Countershading in zebrafish results from an Asip1 controlled dorsoventral gradient of pigment cell differentiation

  2019cites this paper
• Unique evolution of vitamin A as an external pigment in tropical starlings

  2019cites this paper
• Genomic regions of speciation and adaptation among three species of grouse

  2019cites this paper
• Cloudy with a Chance of Insights: Context Dependent Gene Regulation and Implications for Evolutionary Studies

  2019cites this paper
• Genetic and Genomic Bases of Evolved Increases in Stickleback Dentition

  2018influential citation
• Polygenic selection drives the evolution of convergent transcriptomic landscapes across continents within a Nearctic sister-species complex

  2018cites this paper
• COLOURATION AS AN INTRASPECIFIC SIGNAL IN BIRDS

  2018cites this paper
• Allelic polymorphism at foxo contributes to local adaptation in Drosophila melanogaster

  2018cites this paper
• Inverse European Latitudinal Cline at the timeless Locus of Drosophila melanogaster Reveals Selection on a Clock Gene: Population Genetics of ls-tim

  2018cites this paper
• Fish Pigmentation. A Key Issue for the Sustainable Development of Fish Farming

  2018cites this paper
• Molecular identification of colour pattern genes in birds

  2018cites this paper
• Evolution of DNA methylation in Papio baboons

  2018cites this paper
• Function and underlying mechanisms of seasonal colour moulting in mammals and birds: what keeps them changing in a warming world?

  2018cites this paper
• Transcriptome analysis provides insights into the mechanism of albinism during different pigmentation stages of the albino sea cucumber Apostichopus japonicus

  2018cites this paper
• Annual Review of Ecology , Evolution , and Systematics ( Non ) Parallel Evolution

  2018cites this paper
• How fish get their stripes—again and again

  2018cites this paper
• Mutations in the melanocortin-1 receptor (MC1R) gene have no influence on the distinct patterns of melanic plumage found in the manakins of the genus Antilophia (Aves: Pipridae).

  2018cites this paper
• Ancient mechanisms for the evolution of the bicoid homeodomain's function in fly development

  2018cites this paper
• Differential gene regulation underlies variation in melanic plumage coloration in the dark‐eyed junco (Junco hyemalis)

  2018cites this paper
• De Novo assembly and comparative transcriptome analyses of purple and green morphs of Apostichopus japonicus during body wall pigmentation process.

  2018cites this paper
• Animal behaviour and algal camouflage jointly structure predation and selection

  2018cites this paper
• The periodic coloration in birds forms through a prepattern of somite origin

  2018cites this paper
• The developmental and genetic trajectory of coloration in the guppy (Poecilia reticulata)

  2018cites this paper
• Integrative Population and Physiological Genomics Reveals Mechanisms of Adaptation in Killifish

  2018cites this paper
• How a growing organismal perspective is adding new depth to integrative studies of morphological evolution

  2018cites this paper