DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Transcriptomic analysis of skin pigmentation variation in the Virginia opossum ( Didelphis virginiana )

Journal Article · · Molecular Ecology
DOI: https://doi.org/10.1111/mec.14712 · OSTI ID:1440263
ORCiD logo [1];  [2];  [3];  [4];  [5];  [1]
  1. Department of Ecology and Evolutionary Biology University of California, Los Angeles Los Angeles California
  2. Key Lab of Animal Ecology and Conservation Biology Institute of Zoology Chinese Academy of Sciences Chaoyang, Beijing China
  3. Savannah River Ecology Lab Warnell School of Forestry and Natural Resources University of Georgia Aiken South Carolina
  4. Centro de Investigaciones Regionales “Dr. Hideyo Noguchi” Universidad Autónoma de Yucatán Mérida Yucatán Mexico
  5. Departamento de Ecología Evolutiva Centro de Investigación en Biodiversidad y Conservación Universidad Autónoma del Estado de Morelos Cuernavaca Morelos Mexico

Abstract Skin pigmentation and coat pigmentation are two of the best‐studied examples of traits under natural selection given their quantifiable fitness interactions with the environment (e.g., camouflage) and signalling with other organisms (e.g., warning coloration). Previous morphological studies have found that skin pigmentation variation in the Virginia opossum ( Didelphis virginiana ) is associated with variation in precipitation and temperatures across its distribution range following Gloger's rule (lighter pigmentation in temperate environments). To investigate the molecular mechanism associated with skin pigmentation variation, we used RNA‐Seq and quantified gene expression of wild opossums from tropical and temperate populations. Using differential expression analysis and a co‐expression network approach, we found that expression variation in genes with melanocytic and immune functions is significantly associated with the degree of skin pigmentation variation and may be underlying this phenotypic difference. We also found evidence suggesting that the Wnt/β‐catenin signalling pathway might be regulating the depigmentation observed in temperate populations. Based on our study results, we present several alternative hypotheses that may explain Gloger's rule pattern of skin pigmentation variation in opossum, including changes in pathogen diversity supporting a pathogen‐resistant hypothesis, thermal stress associated with temperate environments, and pleiotropic and epistatic interactions between melanocytic and immune genes.

Sponsoring Organization:
USDOE
Grant/Contract Number:
FC09-07SR22506
OSTI ID:
1440263
Journal Information:
Molecular Ecology, Journal Name: Molecular Ecology Journal Issue: 12 Vol. 27; ISSN 0962-1083
Publisher:
Wiley-BlackwellCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (156)

Extensions to pedigree analysis. IV. Covariance components models for multivariate traits journal March 1983
Physiological factors that regulate skin pigmentation journal March 2009
Review and update of mutations causing Waardenburg syndrome journal February 2010
Networks and pathways in pigmentation, health, and disease
  • Baxter, Laura L.; Loftus, Stacie K.; Pavan, William J.
  • Wiley Interdisciplinary Reviews: Systems Biology and Medicine, Vol. 1, Issue 3 https://doi.org/10.1002/wsbm.20
journal November 2009
Isolation, Characterization, and Mapping of Two Human Potassium Channels journal December 1997
The Antimicrobial Properties of Melanocytes, Melanosomes and Melanin and the Evolution of Black Skin journal July 2001
limma: Linear Models for Microarray Data book January 2005
The genetic basis of adaptation: lessons from concealing coloration in pocket mice book January 2005
Introduction book January 2012
The comparative energetics of neotropical marsupials journal January 1978
TissueDistributionDBs: a repository of organism-specific tissue-distribution profiles journal November 2009
The skin barrier as an innate immune element journal March 2007
The Tyr (albino) locus of the laboratory mouse journal October 2004
Cone pigments in a North American marsupial, the opossum (Didelphis virginiana) journal March 2010
The fur of mammals in exposed environments; do crypsis and thermal needs necessarily conflict? The polar bear and marsupial koala compared journal December 2013
The complement system journal September 2010
Social huddling and physiological thermoregulation are related to melanism in the nocturnal barn owl journal November 2015
Sexual selection in genetic colour-polymorphic species: a review of experimental studies and perspectives journal July 2006
MEF up-regulates human β-defensin 2 expression in epithelial cells journal March 2004
Paleoclimate simulations for North America over the past 21,000 years journal April 1998
Cathepsins: Key modulators of cell death and inflammatory responses journal December 2008
Signaling pathways in melanosome biogenesis and pathology journal July 2010
Dishevelled: The hub of Wnt signaling journal May 2010
NDUFA4 Mutations Underlie Dysfunction of a Cytochrome c Oxidase Subunit Linked to Human Neurological Disease journal June 2013
Innate immune mechanisms in vitiligo: danger from within journal December 2013
Animal models of vitiligo: Matching the model to the question journal December 2014
Differential gene expression analysis identifies murine Cacnb3 as strongly upregulated in distinct dendritic cell populations upon stimulation journal February 2011
The two NF-κB activation pathways and their role in innate and adaptive immunity journal June 2004
Expressional changes in the intracellular melanogenesis pathways and their possible role the pathogenesis of vitiligo journal October 2008
New insights into the roles of Stat5a/b and Stat3 in T cell development and differentiation journal August 2008
Pleiotropic effects of coat colour-associated mutations in humans, mice and other mammals journal June 2013
Characterizing natural variation using next-generation sequencing technologies journal October 2009
Vertebrate pigmentation: from underlying genes to adaptive function journal May 2010
Pleiotropy in the melanocortin system, coloration and behavioural syndromes journal September 2008
Microphthalmia-Associated Transcription Factor in the Wnt Signaling Pathway journal June 2003
Mouse Models for Four Types of Waardenburg Syndrome journal October 2003
The Color Loci of Mice - A Genetic Century journal August 2003
Transcriptional and signaling regulation in neural crest stem cell-derived melanocyte development: do all roads lead to Mitf? journal November 2008
Interactome analysis of gene expression profile reveals potential novel key transcriptional regulators of skin pathology in vitiligo journal November 2015
Applications of next generation sequencing in molecular ecology of non-model organisms journal December 2010
Six Decades of Vitiligo Genetics: Genome-Wide Studies Provide Insights into Autoimmune Pathogenesis journal February 2012
Transcriptional Analysis of Vitiligo Skin Reveals the Alteration of WNT Pathway: A Promising Target for Repigmenting Vitiligo Patients journal December 2015
Evidence for dynamically organized modularity in the yeast protein–protein interaction network journal June 2004
Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry journal November 2004
Melanocyte biology and skin pigmentation journal February 2007
Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences journal May 2007
The Genotype-Tissue Expression (GTEx) project journal May 2013
The evolutionary ecology of the major histocompatibility complex journal August 2005
Genetics, development and evolution of adaptive pigmentation in vertebrates journal July 2006
Ecological genomics: understanding gene and genome function in the natural environment journal May 2007
MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?: MHC studies in nonmodel vertebrates journal April 2003
Fur versus feathers: the different roles of red kangaroo fur and emu feathers in thermoregulation in the Australian arid zone. journal January 2004
Genetically-Determined Variation of Pelage Color and Reflectance in Natural and Laboratory Populations of the Marsupial Sminthopsis-Crassicaudata (Gould) journal January 1988
Developmental plasticity and the origin of species differences journal May 2005
Conservation and evolution of gene coexpression networks in human and chimpanzee brains journal November 2006
Analysis of oncogenic signaling networks in glioblastoma identifies ASPM as a molecular target journal November 2006
Human skin pigmentation as an adaptation to UV radiation journal May 2010
Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change journal July 2012
DC-SIGN activation mediates the differential effects of SAP and CRP on the innate immune system and inhibits fibrosis in mice journal June 2015
Statistical significance for genomewide studies journal July 2003
Pax3 and Regulation of the Melanocyte-specific Tyrosinase-related Protein-1 Promoter journal September 1999
Inflammatory Proprotein Convertase-Matrix Metalloproteinase Proteolytic Pathway in Antigen-presenting Cells as a Step to Autoimmune Multiple Sclerosis journal September 2009
Cathepsin H Is an Additional Convertase of Pro-granzyme B journal April 2010
Human Pigmentation and Environmental Adaptation journal November 1965
CD163: a regulated hemoglobin scavenger receptor with a role in the anti‐inflammatory response journal January 2004
Ecological and behavioral correlates of coloration in artiodactyls: systematic analyses of conventional hypotheses journal November 2003
TimeTree: a public knowledge-base of divergence times among organisms journal October 2006
Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R journal November 2007
QuickGO: a web-based tool for Gene Ontology searching journal September 2009
TiSGeD: a database for tissue-specific genes journal March 2010
HTSeq--a Python framework to work with high-throughput sequencing data journal September 2014
Removing technical variability in RNA-seq data using conditional quantile normalization journal January 2012
Calcium‐activated potassium channel SK1‐ and IK1‐like immunoreactivity in injured human sensory neurones and its regulation by neurotrophic factors journal February 2002
Gloger's Rule, Feather-Degrading Bacteria, and Color Variation Among Song Sparrows journal August 2004
Isolation and Mapping of a Putative b Subunit of Human ATP Synthase (ATP-BL) from Human Leukocytes journal January 1999
Genetic Evidence for the Convergent Evolution of Light Skin in Europeans and East Asians journal December 2006
Gene Coexpression Networks Reveal Key Drivers of Phenotypic Divergence in Lake Whitefish journal March 2013
Tree of Life Reveals Clock-Like Speciation and Diversification journal March 2015
g:Profiler—a web server for functional interpretation of gene lists (2011 update) journal June 2011
How the zebra got its stripes: a problem with too many solutions journal January 2015
Compelling evidence that a single nucleotide substitution in TYRP1 is responsible for coat-colour polymorphism in a free-living population of Soay sheep journal December 2006
Evolution of an avian pigmentation gene correlates with a measure of sexual selection journal May 2007
Adaptive evolution of facial colour patterns in Neotropical primates journal January 2012
Convergence in pigmentation at multiple levels: mutations, genes and function
  • Manceau, Marie; Domingues, Vera S.; Linnen, Catherine R.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, Issue 1552 https://doi.org/10.1098/rstb.2010.0104
journal August 2010
Genomics of coloration in natural animal populations journal May 2017
Darwinian and demographic forces affecting human protein coding genes journal March 2009
Gene expression drives local adaptation in humans journal March 2013
Modern vitiligo genetics sheds new light on an ancient disease journal May 2013
Towards the identification of the loci of adaptive evolution journal February 2015
On the measurement and classification of colour in studies of animal colour patterns journal December 1990
Ecogeographical rules: elements of a synthesis journal March 2008
Ecotypic variation in the context of global climate change: revisiting the rules journal July 2006
Autoimmunity as an aetiological factor in vitiligo journal August 2007
The Genetical Structure of Populations journal January 1949
Variation of coat color in house mice throughout Asia journal March 2008
Natural Selection Along an Environmental Gradient: a Classic Cline in Mouse Pigmentation journal July 2008
The correlation of TRPM1 (Melastatin) mRNA expression with microphthalmia-associated transcription factor (MITF) and other melanogenesis-related proteins in normal and pathological skin, hair follicles and melanocytic nevi journal April 2010
A review of genetic disorders of hypopigmentation: lessons learned from the biology of melanocytes journal September 2009
SOX10, in combination with Sp1, regulates the endothelin receptor type B gene in human melanocyte lineage cells journal April 2006
Pleiotropy in the melanocortin system: expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl ( Strix aluco ) journal August 2013
Ten years of transcriptomics in wild populations: what have we learned about their ecology and evolution? journal January 2015
Effect of the MC1R gene on sexual dimorphism in melanin-based colorations journal May 2015
Transcriptomics of colour patterning and coloration shifts in crows journal September 2015
Genetic subdivision and candidate genes under selection in North American grey wolves journal November 2015
The power and promise of RNA-seq in ecology and evolution journal March 2016
MC1R variants affect the expression of melanocortin and melanogenic genes and the association between melanocortin genes and coloration journal October 2016
Seasonal gene expression in a migratory songbird journal November 2016
Genome-wide expression reveals multiple systemic effects associated with detection of anticoagulant poisons in bobcats ( Lynx rufus ) journal March 2018
A Single Amino Acid Mutation Contributes to Adaptive Beach Mouse Color Pattern journal July 2006
Molecular and Evolutionary History of Melanism in North American Gray Wolves journal March 2009
Modeling Effects of Environmental Change on Wolf Population Dynamics, Trait Evolution, and Life History journal December 2011
Adaptive Evolution of Multiple Traits Through Multiple Mutations at a Single Gene journal March 2013
The genomic landscape underlying phenotypic integrity in the face of gene flow in crows journal June 2014
Spatial Response of Mammals to Late Quaternary Environmental Fluctuations journal June 1996
The biology of color journal August 2017
Role of protein kinase C β 2 activation in TNF-α-induced human vascular endothelial cell apoptosis journal March 2009
Variations in MHC Class II Antigen Processing and Presentation in Health and Disease journal May 2016
The wnt Signaling Pathway in Development and Disease journal November 2004
THE NF-κB AND IκB PROTEINS: New Discoveries and Insights journal April 1996
AMPK in Health and Disease journal July 2009
Melanin Pigmentation in Mammalian Skin and Its Hormonal Regulation journal October 2004
Neuroendocrine System of the Skin journal January 2005
Molecular Study of Three Lebanese and Syrian Patients with Waardenburg Syndrome and Report of Novel Mutations in the EDNRB and MITF Genes journal January 2010
“Good Enough Solutions” and the Genetics of Complex Diseases journal August 2012
TiGER: a database for tissue-specific gene expression and regulation journal January 2008
WGCNA: an R package for weighted correlation network analysis journal December 2008
Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits journal January 2011
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions journal January 2013
voom: precision weights unlock linear model analysis tools for RNA-seq read counts journal January 2014
Functional compatibility between isoform   and   of type II DNA topoisomerase journal March 2004
All TRAFs are not created equal: common and distinct molecular mechanisms of TRAF-mediated signal transduction journal February 2002
Nek2A destruction marks APC/C activation at the prophase-to-prometaphase transition by spindle-checkpoint-restricted Cdc20 journal February 2015
Comparative genomics in ecological physiology: toward a more nuanced understanding of acclimation and adaptation journal February 2012
Geometric Interpretation of Gene Coexpression Network Analysis journal August 2008
Integrating Genetic and Network Analysis to Characterize Genes Related to Mouse Weight journal January 2006
A Systems Genetics Approach Implicates USF1, FADS3, and Other Causal Candidate Genes for Familial Combined Hyperlipidemia journal September 2009
Adaptations to Climate-Mediated Selective Pressures in Humans journal April 2011
Transcriptome Analysis Reveals Markers of Aberrantly Activated Innate Immunity in Vitiligo Lesional and Non-Lesional Skin journal December 2012
Antibacterial Properties of the Mammalian L-Amino Acid Oxidase IL4I1 journal January 2013
When Is Hub Gene Selection Better than Standard Meta-Analysis? journal April 2013
Snowflake Vitreoretinal Degeneration (SVD) Mutation R162W Provides New Insights into Kir7.1 Ion Channel Structure and Function journal August 2013
Scavenger Receptor CD163 and Its Biological Functions journal January 2009
A Systems Level Analysis of Transcriptional Changes in Alzheimer's Disease and Normal Aging journal February 2008
Differential Gene Expression of TRPM1 , the Potential Cause of Congenital Stationary Night Blindness and Coat Spotting Patterns ( LP ) in the Appaloosa Horse ( Equus caballus ) journal July 2008
The complement system: History, pathways, cascade and inhibitors journal June 2012
The Adaptive Significance of Coloration in Mammals journal January 2005
Identification of the oncogenic kinase TOPK/PBK as a master mitotic regulator of C2H2 zinc finger proteins journal January 2015
A General Framework for Weighted Gene Co-Expression Network Analysis journal January 2005
The Adaptiveness of Animal Colors journal November 1981
The Prehistoric Distribution of the Opossum journal February 1958
Didelphis virginiana journal May 1974
Emerging infectious disease selects for darker plumage coloration in greenfinches journal March 2014
MHC Class II Polymorphisms, Autoreactive T-Cells, and Autoimmunity journal January 2013
SKAP associates with kinetochores and promotes the metaphase-to-anaphase transition journal September 2009
CDK5RAP2 is required for spindle checkpoint function journal April 2009
Playing by the rules? Phenotypic adaptation to temperate environments in an American marsupial journal January 2018