Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird

Soulsbury CD, Lipponen A, Wood K, Mein CA, Hoffman J, Lebigre C (2018)
Ecology and Evolution 8(13): 1-11.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
OA 907.45 KB
Soulsbury, Carl D.; Lipponen, Anssi; Wood, Kristie; Mein, Charles A.; Hoffman, JosephUniBi ; Lebigre, Christophe
Abstract / Bemerkung
Secondary sexual trait expression can be influenced by fixed individual factors (such as genetic quality) as well as by dynamic factors (such as age and environmentally induced gene expression) that may be associated with variation in condition or quality. In particular, melanin‐based traits are known to relate to condition and there is a well‐characterized genetic pathway underpinning their expression. However, the mechanisms linking variable trait expression to genetic quality remain unclear. One plausible mechanism is that genetic quality could influence trait expression via differential methylation and differential gene expression. We therefore conducted a pilot study examining DNA methylation at a candidate gene (agouti‐related neuropeptide: AgRP) in the black grouse Lyrurus tetrix. We specifically tested whether CpG methylation covaries with age and multilocus heterozygosity (a proxy of genetic quality) and from there whether the expression of a melanin‐based ornament (ultraviolet‐blue chroma) correlates with DNA methylation. Consistent with expectations, we found clear evidence for age‐ and heterozygosity‐specific patterns of DNA methylation, with two CpG sites showing the greatest DNA methylation in highly heterozygous males at their peak age of reproduction. Furthermore, DNA methylation at three CpG sites was significantly positively correlated with ultraviolet‐blue chroma. Ours is the first study to our knowledge to document age‐ and quality‐dependent variation in DNA methylation and to show that dynamic sexual trait expression across the lifespan of an organism is associated with patterns of DNA methylation. Although we cannot demonstrate causality, our work provides empirical support for a mechanism that could potentially link key individual factors to variation in sexual trait expression in a wild vertebrate.
Ecology and Evolution
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Soulsbury CD, Lipponen A, Wood K, Mein CA, Hoffman J, Lebigre C. Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird. Ecology and Evolution. 2018;8(13):1-11.
Soulsbury, C. D., Lipponen, A., Wood, K., Mein, C. A., Hoffman, J., & Lebigre, C. (2018). Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird. Ecology and Evolution, 8(13), 1-11. doi:10.1002/ece3.4132
Soulsbury, Carl D., Lipponen, Anssi, Wood, Kristie, Mein, Charles A., Hoffman, Joseph, and Lebigre, Christophe. 2018. “Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird”. Ecology and Evolution 8 (13): 1-11.
Soulsbury, C. D., Lipponen, A., Wood, K., Mein, C. A., Hoffman, J., and Lebigre, C. (2018). Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird. Ecology and Evolution 8, 1-11.
Soulsbury, C.D., et al., 2018. Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird. Ecology and Evolution, 8(13), p 1-11.
C.D. Soulsbury, et al., “Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird”, Ecology and Evolution, vol. 8, 2018, pp. 1-11.
Soulsbury, C.D., Lipponen, A., Wood, K., Mein, C.A., Hoffman, J., Lebigre, C.: Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird. Ecology and Evolution. 8, 1-11 (2018).
Soulsbury, Carl D., Lipponen, Anssi, Wood, Kristie, Mein, Charles A., Hoffman, Joseph, and Lebigre, Christophe. “Age- and quality-dependent DNA methylation correlate with melanin-based coloration in a wild bird”. Ecology and Evolution 8.13 (2018): 1-11.
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80 References

Daten bereitgestellt von Europe PubMed Central.

Testosterone and male mating success on the black grouse leks

A test of the hypothesis of mate choice based on heterozygosity in the spotless starling
Expression of DNA methyltransferases is influenced by growth hormone in the long-living Ames dwarf mouse in vivo and in vitro.
Armstrong VL, Rakoczy S, Rojanathammanee L, Brown-Borg HM., J. Gerontol. A Biol. Sci. Med. Sci. 69(8), 2013
PMID: 24201695
Determinants of age-dependent change in a secondary sexual character.
Balbontin J, De Lope F, Hermosell IG, Mousseau TA, Moller AP., J. Evol. Biol. 24(2), 2010
PMID: 21175908
Fitting linear mixed‐effects models using lme4
Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population.
Bell JT, Tsai PC, Yang TP, Pidsley R, Nisbet J, Glass D, Mangino M, Zhai G, Zhang F, Valdes A, Shin SY, Dempster EL, Murray RM, Grundberg E, Hedman AK, Nica A, Small KS; MuTHER Consortium, Dermitzakis ET, McCarthy MI, Mill J, Spector TD, Deloukas P, Ahmadi KR, Ainali C, Barrett A, Bataille V, Bell JT, Buil A, Deloukas P, Dermitzakis ET, Dimas AS, Durbin R, Glass D, Grundberg E, Hassanali N, Hedman AK, Ingle C, Knowles D, Krestyaninova M, Lindgren CM, Lowe CE, McCarthy MI, Meduri E, di Meglio P, Min JL, Montgomery SB, Nestle FO, Nica AC, Nisbet J, O'Rahilly S, Parts L, Potter S, Sekowska M, Shin SY, Small KS, Soranzo N, Spector TD, Surdulescu G, Travers ME, Tsaprouni L, Tsoka S, Wilk A, Yang TP, Zondervan KT., PLoS Genet. 8(4), 2012
PMID: 22532803
Perceptions of epigenetics.
Bird A., Nature 447(7143), 2007
PMID: 17522671
Decline in genomic DNA methylation through aging in a cohort of elderly subjects.
Bollati V, Schwartz J, Wright R, Litonjua A, Tarantini L, Suh H, Sparrow D, Vokonas P, Baccarelli A., Mech. Ageing Dev. 130(4), 2008
PMID: 19150625
Candidate Gene Analysis Suggests Untapped Genetic Complexity in Melanin-Based Pigmentation in Birds.
Bourgeois YX, Bertrand JA, Delahaie B, Cornuault J, Duval T, Mila B, Thebaud C., J. Hered. 107(4), 2016
PMID: 26995742
Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context.
Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, Nelson HH, Karagas MR, Padbury JF, Bueno R, Sugarbaker DJ, Yeh RF, Wiencke JK, Kelsey KT., PLoS Genet. 5(8), 2009
PMID: 19680444
Beyond DNA: integrating inclusive inheritance into an extended theory of evolution.
Danchin E, Charmantier A, Champagne FA, Mesoudi A, Pujol B, Blanchet S., Nat. Rev. Genet. 12(7), 2011
PMID: 21681209

Gene and transposable element methylation in great tit (Parus major) brain and blood.
Derks MF, Schachtschneider KM, Madsen O, Schijlen E, Verhoeven KJ, van Oers K., BMC Genomics 17(), 2016
PMID: 27146629
Pleiotropy in the melanocortin system, coloration and behavioural syndromes.
Ducrest AL, Keller L, Roulin A., Trends Ecol. Evol. (Amst.) 23(9), 2008
PMID: 18644658
Multiple sexual ornaments signal heterozygosity in male blue tits
Ferrer ES, Garcia‐Navas V, Bueno‐Enciso J, Sanz JJ, Ortego J., Biol. J. Linn. Soc. Lond. 115(2), 2015
PMID: IND601259377
Females increase offspring heterozygosity and fitness through extra-pair matings.
Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B., Nature 425(6959), 2003
PMID: 14562103
Morph-specific genetic and environmental variation in innate and acquired immune response in a color polymorphic raptor.
Gangoso L, Roulin A, Ducrest AL, Grande JM, Figuerola J., Oecologia 178(4), 2015
PMID: 25834999
Analysis of age-related global DNA methylation in chicken.
Gryzinska M, Blaszczak E, Strachecka A, Jezewska-Witkowska G., Biochem. Genet. 51(7-8), 2013
PMID: 23553491
Association between body weight and age of dogs and global DNA methylation
On the correlation between heterozygosity and fitness in natural populations.
Hansson B, Westerberg L., Mol. Ecol. 11(12), 2002
PMID: 12453232
Heterozygosity and orange coloration are associated in the guppy (Poecilia reticulata).
Herdegen M, Dudka K, Radwan J., J. Evol. Biol. 27(1), 2013
PMID: 24329722
Inbreeding depression and male fitness in black grouse.
Hoglund J, Piertney SB, Alatalo RV, Lindell J, Lundberg A, Rintamaki PT., Proc. Biol. Sci. 269(1492), 2002
PMID: 11934362
DNA methylation age of human tissues and cell types.
Horvath S., Genome Biol. 14(10), 2013
PMID: 24138928
Epigenetic inheritance and plasticity: The responsive germline.
Jablonka E., Prog. Biophys. Mol. Biol. 111(2-3), 2012
PMID: 22975443
Sexually selected traits: a fundamental framework for studies on behavioral epigenetics.
Jasarevic E, Geary DC, Rosenfeld CS., ILAR J 53(3-4), 2012
PMID: 23744965
Senescence rates are determined by ranking on the fast-slow life-history continuum.
Jones OR, Gaillard JM, Tuljapurkar S, Alho JS, Armitage KB, Becker PH, Bize P, Brommer J, Charmantier A, Charpentier M, Clutton-Brock T, Dobson FS, Festa-Bianchet M, Gustafsson L, Jensen H, Jones CG, Lillandt BG, McCleery R, Merila J, Neuhaus P, Nicoll MA, Norris K, Oli MK, Pemberton J, Pietiainen H, Ringsby TH, Roulin A, Saether BE, Setchell JM, Sheldon BC, Thompson PM, Weimerskirch H, Jean Wickings E, Coulson T., Ecol. Lett. 11(7), 2008
PMID: 18445028
Determinants of yearling male lekking effort and mating success in black grouse (Tetrao tetrix)
Life-history differences in age-dependent expressions of multiple ornaments and behaviors in a lekking bird.
Kervinen M, Lebigre C, Alatalo RV, Siitari H, Soulsbury CD., Am. Nat. 185(1), 2014
PMID: 25560550

Evolutionary signals of selection on cognition from the great tit genome and methylome.
Laine VN, Gossmann TI, Schachtschneider KM, Garroway CJ, Madsen O, Verhoeven KJ, de Jager V, Megens HJ, Warren WC, Minx P, Crooijmans RP, Corcoran P; Great Tit HapMap Consortium, Sheldon BC, Slate J, Zeng K, van Oers K, Visser ME, Groenen MA, Adriaensen F, Belda E, Bushuev A, Cichon M, Charmantier A, Dingemanse N, Doligez B, Eeva T, Erikstad KE, Fedorov S, Hau M, Hille S, Hinde C, Kempenaers B, Kerimov A, Krist M, Mand R, Matthysen E, Nager R, Norte C, Orell M, Richner H, Slagsvold T, Tilgar V, Tinbergen J, Torok J, Tschirren B, Yuta T., Nat Commun 7(), 2016
PMID: 26805030
Leucocyte counts variation and measures of male fitness in the lekking black grouse
Restrictive mating by females on black grouse leks.
Lebigre C, Alatalo RV, Siitari H, Parri S., Mol. Ecol. 16(20), 2007
PMID: 17850264
Patterns of DNA methylation throughout a range expansion of an introduced songbird.
Liebl AL, Schrey AW, Richards CL, Martin LB., Integr. Comp. Biol. 53(2), 2013
PMID: 23535948
JASPAR 2016: A major expansion and update of the open‐access database of transcription factor binding profiles
Differential expression of a new dominant agouti allele (Aiapy) is correlated with methylation state and is influenced by parental lineage.
Michaud EJ, van Vugt MJ, Bultman SJ, Sweet HO, Davisson MT, Woychik RP., Genes Dev. 8(12), 1994
PMID: 7926745
Testosterone, immunocompetence, and honest sexual signaling in male red grouse
Parasites, testosterone and honest carotenoid-based signalling of health
PMID: IND43947628
Evolution of an avian pigmentation gene correlates with a measure of sexual selection.
Nadeau NJ, Burke T, Mundy NI., Proc. Biol. Sci. 274(1620), 2007
PMID: 17504743
Inter- and intrasexual variation in aging patterns across reproductive traits in a wild red deer population.
Nussey DH, Kruuk LE, Morris A, Clements MN, Pemberton JM, Clutton-Brock TH., Am. Nat. 174(3), 2009
PMID: 19653847
Pheasant sexual ornaments reflect nutritional conditions during early growth.
Ohlsson T, Smith HG, Raberg L, Hasselquist D., Proc. Biol. Sci. 269(1486), 2002
PMID: 11788032
Conserved distal promoter of the agouti signaling protein (ASIP) gene controls sexual dichromatism in chickens.
Oribe E, Fukao A, Yoshihara C, Mendori M, Rosal KG, Takahashi S, Takeuchi S., Gen. Comp. Endocrinol. 177(2), 2012
PMID: 22554923
Measuring Animal Age with DNA Methylation: From Humans to Wild Animals.
De Paoli-Iseppi R, Deagle BE, McMahon CR, Hindell MA, Dickinson JL, Jarman SN., Front Genet 8(), 2017
PMID: 28878806
Low heterozygosity at microsatellite markers in Iberian red deer with small antlers.
Perez-Gonzalez J, Carranza J, Torres-Porras J, Fernandez-Garcia JL., J. Hered. 101(5), 2010
PMID: 20478822
Epigenetic estimation of age in humpback whales.
Polanowski AM, Robbins J, Chandler D, Jarman SN., Mol Ecol Resour 14(5), 2014
PMID: 24606053

Inherited epigenetic variation--revisiting soft inheritance.
Richards EJ., Nat. Rev. Genet. 7(5), 2006
PMID: 16534512
Genetics of colouration in birds.
Roulin A, Ducrest AL., Semin. Cell Dev. Biol. 24(6-7), 2013
PMID: 23665152
Sex-specific fitness effects of unpredictable early life conditions are associated with DNA methylation in the avian glucocorticoid receptor.
Rubenstein DR, Skolnik H, Berrio A, Champagne FA, Phelps S, Solomon J., Mol. Ecol. 25(8), 2016
PMID: 26588348
MC1R variants affect the expression of melanocortin and melanogenic genes and the association between melanocortin genes and coloration.
San-Jose LM, Ducrest AL, Ducret V, Simon C, Richter H, Wakamatsu K, Roulin A., Mol. Ecol. 26(1), 2016
PMID: 27664794
Condition dependence of a multicomponent sexual signal in the field cricket Gryllus campestris
Color signals in the black grouse (Tetrao tetrix): signal properties and their condition dependency.
Siitari H, Alatalo RV, Halme P, Buchanan KL, Kilpimaa J., Am. Nat. 169 Suppl 1(), 2007
PMID: 19426093
Age-dependent inbreeding risk and offspring fitness costs in female black grouse.
Soulsbury CD, Alatalo RV, Lebigre C, Rokka K, Siitari H., Biol. Lett. 7(6), 2011
PMID: 21632620
Curse of the black spot: Spotting negatively correlates with fitness in black grouse Lyrurus tetrix
Viability selection creates negative heterozygosity–fitness correlations in female Black Grouse Lyrurus tetrix
Age-associated changes in DNA methylation across multiple tissues in an inbred mouse model.
Spiers H, Hannon E, Wells S, Williams B, Fernandes C, Mill J., Mech. Ageing Dev. 154(), 2016
PMID: 26861500
inbreedR: An R package for the analysis of inbreeding based on genetic markers
DNA methylation landscapes: provocative insights from epigenomics.
Suzuki MM, Bird A., Nat. Rev. Genet. 9(6), 2008
PMID: 18463664
High parasite load in house finches (Carpodacus mexicanus) is correlated with reduced expression of a sexually selected trait
Epigenetic mechanisms underlying developmental plasticity in horned beetles.
Valena S, Moczek AP., Genet Res Int 2012(), 2012
PMID: 22567393
Evidence from pyrosequencing indicates that natural variation in animal personality is associated with DRD4 DNA methylation.
Verhulst EC, Mateman AC, Zwier MV, Caro SP, Verhoeven KJ, van Oers K., Mol. Ecol. 25(8), 2016
PMID: 26678756
Age-dependent genetic effects on a secondary sexual trait in male Alpine ibex, Capra ibex.
Von Hardenberg A, Bassano B, Festa-Bianchet M, Luikart G, Lanfranchi P, Coltman D., Mol. Ecol. 16(9), 2007
PMID: 17444905
Impact of cytosine methylation on DNA binding specificities of human transcription factors.
Yin Y, Morgunova E, Jolma A, Kaasinen E, Sahu B, Khund-Sayeed S, Das PK, Kivioja T, Dave K, Zhong F, Nitta KR, Taipale M, Popov A, Ginno PA, Domcke S, Yan J, Schubeler D, Vinson C, Taipale J., Science 356(6337), 2017
PMID: 28473536

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