Genetic and Epigenetic Differentiation in Response to Genomic Selection for Avian Lay Date
Open accessAbstract
Anthropogenic climate change has led to globally increasing temperatures at an unprecedented pace and, to persist, wild species have to adapt to their changing world. We, however, often fail to derive reliable predictions of species' adaptive potential. Genomic selection represents a powerful tool to investigate the adaptive potential of a species, but constitutes a ‘blind process’ with regard to the underlying genomic architecture of the relevant phenotypes. Here, we used great tit (Parus major) females from a genomic selection experiment for avian lay date to zoom into this blind process. We aimed to identify the genetic variants that responded to genomic selection and epigenetic variants that accompanied this response and, this way, might reflect heritable genetic variation at the epigenetic level. We applied whole genome bisulfite sequencing to blood samples of individual great tit females from the third generation of bidirectional genomic selection lines for early and late lay date. Genomic selection resulted in differences at both the genetic and epigenetic level. Genetic variants that showed signatures of selection were located within genes mostly linked to brain development and functioning, including LOC107203824 (SOX3‐like). SOX3 is a transcription factor that is required for normal hypothalamo‐pituitary axis development and functioning, an essential part of the reproductive axis. As for epigenetic differentiation, the early selection line showed hypomethylation relative to the late selection line. Sites with differential DNA methylation were located in genes important for various biological processes, including gonadal functioning (e.g., MSTN and PIK3CB). Overall, genomic selection for avian lay date provided insights into where within the genome the heritable genetic variation for lay date, on which selection can operate, resides and indicates that some of this variation might be reflected by epigenetic variants.
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Genetic variation remains stable throughout the sexual cycle or repeated asexual propagation, whereas epigenetic variation may be unstable even during asexual propagation.
“Genetic variation remains stable throughout the sexual cycle or repeated asexual propagation, whereas epigenetic variation may be unstable even during asexual propagation [29].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [29]
The Discussion (page unavailable) says there is limited evidence for stable inheritance of spontaneous epigenetic mutations in vertebrates and describes DNA-methylation reprogramming during fertilization. It does not establish that genetic variation remains stable across sexual cycles or repeated asexual propagation, or that epigenetic variation is unstable during asexual propagation. (LLM, conf=0.78)
Experimental — accuracy not yet measuredIn plant tissue culture, stress conditions can influence epigenetic stability and genetic makeup, often triggering epigenetic modifications that regulate plant responses to environmental cues.
“In plant tissue culture, stress conditions can influence the epigenetic stability and genetic makeup of plant materials, often triggering epigenetic modifications that regulate plant responses to environmental cues [29,50].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [29]
The Introduction (page not specified) discusses environmentally induced epigenetic modifications and describes epigenetic processes as responsive to the environment in maize. It does not address plant tissue culture or show that culture-related stress changes the epigenetic stability or genetic makeup of plant materials. (LLM, conf=0.85)
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Epigenetic inheritance and the missing heritability
Trerotola, M., Relli, V., Simeone, P., & Alberti, S. (2015) · Human Genomics · doi:10.1186/s40246-015-0041-3 · Cited by 318 · cited 1× · see citing works
“Epigenetics marks, that is chemical modifications of the DNA sequences or DNA-associated histones, are suggested to con - tribute to heritable phenotypic variation (Trerotola et al., 2015 ).”
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Research works printed but not linked: 115
- Akalin, A., Kormaksson, M., Li, S., Garrett‐Bakelman, F. E., Figueroa, M. E., Melnick, A., & Mason, C. E. (2012). methylKit: A comprehensive R package for the analysis of genome‐wide DNA methylation profiles. Genome Biology, 13, R87. 10.1186/gb-2012-13-10-r87 23034086 PMC3491415 · DOI
- Arming, S., Wipfler, D., Mayr, J., Merling, A., Vilas, U., Schauer, R., Schwartz‐Albiez, R., & Vlasak, R. (2011). The human Cas1 protein: A sialic acid‐specific O‐acetyltransferase? Glycobiology, 21, 553– 564. 10.1093/glycob/cwq153 20947662 PMC7108626 · DOI
- Aulchenko, Y. S., Ripke, S., Isaacs, A., & van Duijn, C. M. (2007). GenABEL: An R library for genome‐wide association analysis. Bioinformatics, 23, 1294– 1296. 10.1093/bioinformatics/btm108 17384015 · DOI · Paper page
- Barson, N. J., Aykanat, T., Hindar, K., Baranski, M., Bolstad, G. H., Fiske, P., Jacq, C., Jensen, A. J., Johnston, S. E., Karlsson, S., Kent, M., Moen, T., Niemelä, E., Nome, T., Næsje, T. F., Orell, P., Romakkaniemi, A., Sægrov, H., Urdal, K., … Primmer, C. R. (2015). Sex‐dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature, 528, 405– 408. 10.1038/nature16062 26536110 · DOI
- Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67, 1– 48. 10.18637/jss.v067.i01 · DOI · Paper page
- Bellinge, R. H. S., Liberles, D. A., Iaschi, S. P. A., O'Brien, P. A., & Tay, G. K. (2005). Myostatin and its implications on animal breeding: A review. Animal Genetics, 36, 1– 6. 10.1111/j.1365-2052.2004.01229.x 15670124 · DOI
- Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B: Methodological, 57, 289– 300. 10.1111/j.2517-6161.1995.tb02031.x · DOI · Paper page
- Bian, X., Xie, Q., Zhou, Y., Wu, H., Cui, J., Jia, L., & Suo, L. (2021). Transcriptional changes of mouse ovary during follicle initial or cyclic recruitment mediated by extra hormone treatment. Life Sciences, 264, 118654. 10.1016/j.lfs.2020.118654 33141043 · DOI
- Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W.‐H., Pagès, F., Trajanoski, Z., & Galon, J. (2009). ClueGO: A Cytoscape plug‐in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics, 25, 1091– 1093. 10.1093/bioinformatics/btp101 19237447 PMC2666812 · DOI · Paper page
- Bosse, M., Spurgin, L. G., Laine, V. N., Cole, E. F., Firth, J. A., Gienapp, P., Gosler, A. G., McMahon, K., Poissant, J., Verhagen, I., Groenen, M. A. M., van Oers, K., Sheldon, B. C., Visser, M. E., & Slate, J. (2017). Recent natural selection causes adaptive evolution of an avian polygenic trait. Science, 358, 365– 368. 10.1126/science.aal3298 29051380 · DOI
- Burgers, P. P., Bruystens, J., Burnley, R. J., Nikolaev, V. O., Keshwani, M., Wu, J., Janssen, B. J. C., Taylor, S. S., Heck, A. J. R., & Scholten, A. (2016). Structure of smAKAP and its regulation by PKA‐mediated phosphorylation. The FEBS Journal, 283, 2132– 2148. 10.1111/febs.13726 27028580 PMC4980077 · DOI
- Caizergues, A. E., Le Luyer, J., Grégoire, A., Szulkin, M., Senar, J., Charmantier, A., & Perrier, C. (2022). Epigenetics and the city: Non‐parallel DNA methylation modifications across pairs of urban‐forest great tit populations. Evolutionary Applications, 15, 149– 165. 10.1111/eva.13334 35126653 PMC8792475 · DOI
- Cantley, L. C. (2002). The phosphoinositide 3‐kinase pathway. Science, 296, 1655– 1657. 10.1126/science.296.5573.1655 12040186 · DOI · Paper page
- Caro, S. P., Schaper, S. V., Hut, R. A., Ball, G. F., & Visser, M. E. (2013). The case of the missing mechanism: How does temperature influence seasonal timing in endotherms? PLoS Biology, 11, e1001517. 10.1371/journal.pbio.1001517 23565055 PMC3614498 · DOI
- Chang, N.‐Y., Chan, Y.‐J., Ding, S.‐T., Lee, Y.‐H., HuangFu, W.‐C., & Liu, I.‐H. (2016). Sterol O‐acyltransferase 2 contributes to the yolk cholesterol trafficking during zebrafish embryogenesis. PLoS One, 11, e0167644. 10.1371/journal.pone.0167644 27936201 PMC5147938 · DOI
- Charmantier, A., Garant, D., & Kruuk, L. E. B. (2014). Quantitative genetics in the wild. Oxford University Press.
- Charmantier, A., & Gienapp, P. (2014). Climate change and timing of avian breeding and migration: Evolutionary versus plastic changes. Evolutionary Applications, 7, 15– 28. 10.1111/eva.12126 24454545 PMC3894895 · DOI
- Chen, Y.‐J., Hsiao, P.‐W., Lee, M.‐T., Mason, J. I., Ke, F.‐C., & Hwang, J.‐J. (2007). Interplay of PI3K and cAMP/PKA signaling, and rapamycin‐hypersensitivity in TGFβ1 enhancement of FSH‐stimulated steroidogenesis in rat ovarian granulosa cells. Journal of Endocrinology, 192, 405– 419. 10.1677/JOE-06-0076 17283241 · DOI
- Danecek, P., Bonfield, J. K., Liddle, J., Marshall, J., Ohan, V., Pollard, M. O., Whitwham, A., Keane, T., McCarthy, S. A., Davies, R. M., & Li, H. (2021). Twelve years of SAMtools and BCFtools. GigaScience, 10, giab008. 10.1093/gigascience/giab008 33590861 PMC7931819 · DOI
- Dawson, A., King, V. M., Bentley, G. E., & Ball, G. F. (2001). Photoperiodic control of seasonality in birds. Journal of Biological Rhythms, 16, 365– 380. 10.1177/074873001129002079 11506381 · DOI
- DePristo, M. A., Banks, E., Poplin, R., Garimella, K. V., Maguire, J. R., Hartl, C., Philippakis, A. A., del Angel, G., Rivas, M. A., Hanna, M., McKenna, A., Fennell, T. J., Kernytsky, A. M., Sivachenko, A. Y., Cibulskis, K., Gabriel, S. B., Altshuler, D., & Daly, M. J. (2011). A framework for variation discovery and genotyping using next‐generation DNA sequencing data. Nature Genetics, 43, 491– 498. 10.1038/ng.806 21478889 PMC3083463 · DOI
- Derks, M. F. L., Schachtschneider, K. M., Madsen, O., Schijlen, E., Verhoeven, K. J. F., & van Oers, K. (2016). Gene and transposable element methylation in great tit (Parus major) brain and blood. BMC Genomics, 17, 332. 10.1186/s12864-016-2653-y 27146629 PMC4855439 · DOI
- Drent, P. J., van Oers, K., & van Noordwijk, A. J. (2003). Realized heritability of personalities in the great tit (Parus major). Proceedings of the Royal Society of London B, 270, 45– 51. 10.1098/rspb.2002.2168 PMC1691215 12590770 · DOI
- Dubin, M. J., Zhang, P., Meng, D., Remigereau, M.‐S., Osborne, E. J., Paolo Casale, F., Drewe, P., Kahles, A., Jean, G., Vilhjálmsson, B., Jagoda, J., Irez, S., Voronin, V., Song, Q., Long, Q., Rätsch, G., Stegle, O., Clark, R. M., & Nordborg, M. (2015). DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife, 4, e05255. 10.7554/eLife.05255 25939354 PMC4413256 · DOI
- Ewels, P., Magnusson, M., Lundin, S., & Käller, M. (2016). MultiQC: Summarize analysis results for multiple tools and samples in a single report. Bioinformatics, 32, 3047– 3048. 10.1093/bioinformatics/btw354 27312411 PMC5039924 · DOI · Paper page
- Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and windows. Molecular Ecology Resources, 10, 564– 567. 10.1111/j.1755-0998.2010.02847.x 21565059 · DOI
- Feil, R., & Fraga, M. F. (2012). Epigenetics and the environment: Emerging patterns and implications. Nature Reviews. Genetics, 13, 97– 109. 10.1038/nrg3142 22215131 · DOI · Paper page
- Foll, M., & Gaggiotti, O. (2008). A genome‐scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics, 180, 977– 993. 10.1534/genetics.108.092221 18780740 PMC2567396 · DOI
- Forester, B. R., Jones, M. R., Joost, S., Landguth, E. L., & Lasky, J. R. (2016). Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes. Molecular Ecology, 25, 104– 120. 10.1111/mec.13476 26576498 · DOI
- Garcia‐Galiano, D., Borges, B. C., Allen, S. J., & Elias, C. F. (2019). pi 3K signalling in leptin receptor cells: Role in growth and reproduction. Journal of Neuroendocrinology, 31, e12685. 10.1111/jne.12685 30618188 PMC6533139 · DOI
- Garcia‐Galiano, D., Borges, B. C., Donato, J., Allen, S. J., Bellefontaine, N., Wang, M., Zhao, J. J., Kozloff, K. M., Hill, J. W., & Elias, C. F. (2017). PI3Kα inactivation in leptin receptor cells increases leptin sensitivity but disrupts growth and reproduction. JCI Insight, 2, e96728. 10.1172/jci.insight.96728 29212950 PMC5752267 · DOI
- Gienapp, P., Calus, M. P. L., Laine, V. N., & Visser, M. E. (2019). Genomic selection on breeding time in a wild bird population. Evolution Letters, 3, 142– 151. 10.1002/evl3.103 31289689 PMC6591552 · DOI
- Gienapp, P., Laine, V. N., Mateman, A. C., van Oers, K., & Visser, M. E. (2017). Environment‐dependent genotype‐phenotype associations in avian breeding time. Frontiers in Genetics, 8, 102. 10.3389/fgene.2017.00102 28824697 PMC5543038 · DOI
- Grant, P. R., & Grant, B. R. (1995). Predicting microevolutionary responses to directional selection on heritable variation. Evolution, 49, 241– 251. 10.1111/j.1558-5646.1995.tb02236.x 28565006 · DOI
- Grobet, L., Royo Martin, L. J., Poncelet, D., Pirottin, D., Brouwers, B., Riquet, J., Schoeberlein, A., Dunner, S., Ménissier, F., Massabanda, J., Fries, R., Hanset, R., & Georges, M. (1997). A deletion in the bovine myostatin gene causes the double–muscled phenotype in cattle. Nature Genetics, 17, 71– 74. 10.1038/ng0997-71 9288100 · DOI · Paper page
- Gruber, B., Unmack, P. J., Berry, O. F., & Georges, A. (2018). dartr: An r package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources, 18, 691– 699. 10.1111/1755-0998.12745 29266847 · DOI
- Gu, H., Smith, Z. D., Bock, C., Boyle, P., Gnirke, A., & Meissner, A. (2011). Preparation of reduced representation bisulfite sequencing libraries for genome‐scale DNA methylation profiling. Nature Protocols, 6, 468– 481. 10.1038/nprot.2010.190 21412275 · DOI
- Guo, W., Zhu, P., Pellegrini, M., Zhang, M. Q., Wang, X., & Ni, Z. (2018). CGmapTools improves the precision of heterozygous SNV calls and supports allele‐specific methylation detection and visualization in bisulfite‐sequencing data. Bioinformatics, 34, 381– 387. 10.1093/bioinformatics/btx595 28968643 PMC6454434 · DOI · Paper page
- Han, S., Li, Z., Paek, H., Choe, H., Yin, X., & Quan, B. (2021). Reproduction traits of heterozygous myostatin knockout sows crossbred with homozygous myostatin knockout boars. Reproduction in Domestic Animals, 56, 26– 33. 10.1111/rda.13845 33075164 · DOI
- Hill, W. G., & Caballero, A. (1992). Artificial selection experiments. Annual Review of Ecology and Systematics, 23, 287– 310.
- Höglund, A., Henriksen, R., Fogelholm, J., Churcher, A. M., Guerrero‐Bosagna, C. M., Martinez‐Barrio, A., Johnsson, M., Jensen, P., & Wright, D. (2020). The methylation landscape and its role in domestication and gene regulation in the chicken. Nature Ecology & Evolution, 4, 1713– 1724. 10.1038/s41559-020-01310-1 32958860 PMC7616959 · DOI
- Hong, Q., Li, C., Ying, R., Lin, H., Li, J., Zhao, Y., Cheng, H., & Zhou, R. (2019). Loss‐of‐function of sox3 causes follicle development retardation and reduces fecundity in zebrafish. Protein & Cell, 10, 347– 364. 10.1007/s13238-018-0603-y 30588557 PMC6468042 · DOI
- Husby, A., Kawakami, T., Rönnegård, L., Smeds, L., Ellegren, H., & Qvarnström, A. (2015). Genome‐wide association mapping in a wild avian population identifies a link between genetic and phenotypic variation in a life‐history trait. Proceedings of the Royal Society B, 282, 20150156. 10.1098/rspb.2015.0156 25833857 PMC4426624 · DOI
- Jannink, J.‐L., Lorenz, A. J., & Iwata, H. (2010). Genomic selection in plant breeding: From theory to practice. Briefings in Functional Genomics, 9, 166– 177. 10.1093/bfgp/elq001 20156985 · DOI
- Johnson, A. L., Bridgham, J. T., & Swenson, J. A. (2001). Activation of the Akt/protein kinase B signaling pathway is associated with granulosa cell survival. Biology of Reproduction, 64, 1566– 1574. 10.1095/biolreprod64.5.1566 11319165 · DOI
- Johnson, A. L., & Woods, D. C. (2009). Dynamics of avian ovarian follicle development: Cellular mechanisms of granulosa cell differentiation. General and Comparative Endocrinology, 163, 12– 17. 10.1016/j.ygcen.2008.11.012 19059411 · DOI
- Johnston, S. E., Bérénos, C., Slate, J., & Pemberton, J. M. (2016). Conserved genetic architecture underlying individual recombination rate variation in a wild population of Soay sheep (Ovis aries). Genetics, 203, 583– 598. 10.1534/genetics.115.185553 27029733 PMC4858801 · DOI
- Jombart, T. (2008). Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403– 1405. 10.1093/bioinformatics/btn129 18397895 · DOI
- Jombart, T., & Ahmed, I. (2011). Adegenet 1.3‐1: New tools for the analysis of genome‐wide SNP data. Bioinformatics, 27, 3070– 3071. 10.1093/bioinformatics/btr521 21926124 PMC3198581 · DOI
- Kim, J. H., Seo, G. H., Kim, G.‐H., Huh, J., Hwang, I. T., Jang, J.‐H., Yoo, H.‐W., & Choi, J.‐H. (2019). Targeted gene panel sequencing for molecular diagnosis of Kallmann syndrome and Normosmic idiopathic hypogonadotropic hypogonadism. Experimental and Clinical Endocrinology & Diabetes, 127, 538– 544. 10.1055/a-0681-6608 30216942 · DOI
- Kim, J. M., Santure, A. W., Barton, H. J., Quinn, J. L., Cole, E. F., Great Tit HapMap Consortium, Visser, M. E., Sheldon, B. C., Groenen, M. A. M., van Oers, K., & Slate, J. (2018). A high‐density SNP chip for genotyping great tit (Parus major) populations and its application to studying the genetic architecture of exploration behaviour. Molecular Ecology Resources, 18, 877– 891. 10.1111/1755-0998.12778 29573186 · DOI
- Kollias, H. D., & McDermott, J. C. (2008). Transforming growth factor‐β and myostatin signaling in skeletal muscle. Journal of Applied Physiology, 104, 579– 587. 10.1152/japplphysiol.01091.2007 18032576 · DOI
- Koster, J., & Rahmann, S. (2012). Snakemake–a scalable bioinformatics workflow engine. Bioinformatics, 28, 2520– 2522. 10.1093/bioinformatics/bts480 22908215 · DOI · Paper page
- Krueger, F., & Andrews, S. R. (2011). Bismark: A flexible aligner and methylation caller for bisulfite‐seq applications. Bioinformatics, 27, 1571– 1572. 10.1093/bioinformatics/btr167 21493656 PMC3102221 · DOI
- Kruuk, L. E. B., Slate, J., Pemberton, J. M., Brotherstone, S., Guinness, F., & Clutton‐Brock, T. (2002). Antler size in red deer: Heritability and selection but no evolution. Evolution, 56, 1683– 1695. 10.1111/j.0014-3820.2002.tb01480.x 12353761 · DOI
- Kruuk, L. E. B., Slate, J., & Wilson, A. J. (2008). New answers for old questions: The evolutionary quantitative genetics of wild animal populations. Annual Review of Ecology, Evolution, and Systematics, 39, 525– 548. 10.1146/annurev.ecolsys.39.110707.173542 · DOI
- Laine, V. N., Gossmann, T. I., Schachtschneider, K. M., Garroway, C. J., Madsen, O., Verhoeven, K. J. F., de Jager, V., Megens, H.‐J., Warren, W. C., Minx, P., Crooijmans, R. P. M. A., Corcoran, P., The Great Tit HapMap Consortium, Sheldon, B. C., Slate, J., Zeng, K., van Oers, K., Visser, M. E., & Groenen, M. A. M. (2016). Evolutionary signals of selection on cognition from the great tit genome and methylome. Nature Communications, 7, 10474. 10.1038/ncomms10474 PMC4737754 26805030 · DOI
- Laine, V. N., Sepers, B., Lindner, M., Gawehns, F., Ruuskanen, S., & Oers, K. (2023). An ecologist's guide for studying DNA methylation variation in wild vertebrates. Molecular Ecology Resources, 23, 1488– 1508. 10.1111/1755-0998.13624 35466564 · DOI
- Langmead, B., & Salzberg, S. L. (2012). Fast gapped‐read alignment with bowtie 2. Nature Methods, 9, 357– 359. 10.1038/nmeth.1923 22388286 PMC3322381 · DOI · Paper page
- Larsen, F., Gundersen, G., Lopez, R., & Prydz, H. (1992). CpG islands as gene markers in the human genome. Genomics, 13, 1095– 1107. 10.1016/0888-7543(92)90024-M 1505946 · DOI · Paper page
- Lawrence, M., Gentleman, R., & Carey, V. (2009). Rtracklayer: An R package for interfacing with genome browsers. Bioinformatics, 25, 1841– 1842. 10.1093/bioinformatics/btp328 19468054 PMC2705236 · DOI
- Lawrence, M., Huber, W., Pagès, H., Aboyoun, P., Carlson, M., Gentleman, R., Morgan, M. T., & Carey, V. J. (2013). Software for computing and annotating genomic ranges. PLoS Computational Biology, 9, e1003118. 10.1371/journal.pcbi.1003118 23950696 PMC3738458 · DOI
- Lea, A. J., Vilgalys, T. P., Durst, P. A. P., & Tung, J. (2017). Maximizing ecological and evolutionary insight in bisulfite sequencing data sets. Nature Ecology & Evolution, 1, 1074– 1083. 10.1038/s41559-017-0229-0 29046582 PMC5656403 · DOI
- Lee, J., Kim, D.‐H., Brower, A. M., Schlachter, I., & Lee, K. (2021). Effects of myostatin mutation on onset of laying, egg production, fertility, and hatchability. Animals, 11, 1935. 10.3390/ani11071935 34209534 PMC8300113 · DOI
- Lee, J., Kim, D.‐H., & Lee, K. (2020). Muscle hyperplasia in Japanese quail by single amino acid deletion in MSTN Propeptide. International Journal of Molecular Sciences, 21, 1504. 10.3390/ijms21041504 32098368 PMC7073117 · DOI
- Li, L., Shi, X., Shi, Y., & Wang, Z. (2021). The signaling pathways involved in ovarian follicle development. Frontiers in Physiology, 12, 730196. 10.3389/fphys.2021.730196 34646156 PMC8504451 · DOI
- Lindner, M., Gawehns, F., te Molder, S., Visser, M. E., Oers, K., & Laine, V. N. (2022). Performance of methods to detect genetic variants from bisulphite sequencing data in a non‐model species. Molecular Ecology Resources, 22, 834– 846. 10.1111/1755-0998.13493 34435438 PMC9290141 · DOI
- Lindner, M., Laine, V. N., Verhagen, I., Viitaniemi, H. M., Visser, M. E., van Oers, K., & Husby, A. (2021). Rapid changes in DNA methylation associated with the initiation of reproduction in a small songbird. Molecular Ecology, 30, 3645– 3659. 10.1111/mec.15803 33453134 PMC8359384 · DOI
- Lindner, M., Ramakers, J. J., Verhagen, I., Tomotani, B. M., Mateman, A. C., Gienapp, P., & Visser, M. E. (2023). Genotypes selected for early and late avian lay date differ in their phenotype, but not fitness, in the wild. Science Advances, 9, eade6350. 10.1126/sciadv.ade6350 37285433 PMC10246905 · DOI
- Lindner, M., Verhagen, I., Viitaniemi, H. M., Laine, V. N., Visser, M. E., Husby, A., & van Oers, K. (2021). Temporal changes in DNA methylation and RNA expression in a small song bird: Within‐ and between‐tissue comparisons. BMC Genomics, 22, 36. 10.1186/s12864-020-07329-9 33413102 PMC7792223 · DOI
- Lotterhos, K. E., & Whitlock, M. C. (2014). Evaluation of demographic history and neutral parameterization on the performance of f st outlier tests. Molecular Ecology, 23, 2178– 2192. 10.1111/mec.12725 24655127 PMC4228763 · DOI
- Luu, K., Bazin, E., & Blum, M. G. B. (2017). Pcadapt: An r package to perform genome scans for selection based on principal component analysis. Molecular Ecology Resources, 17, 67– 77. 10.1111/1755-0998.12592 27601374 · DOI
- Marrot, P., Charmantier, A., Blondel, J., & Garant, D. (2018). Current spring warming as a driver of selection on reproductive timing in a wild passerine. The Journal of Animal Ecology, 87, 754– 764. 10.1111/1365-2656.12794 29337354 PMC5899892 · DOI
- McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., & DePristo, M. A. (2010). The genome analysis toolkit: A MapReduce framework for analyzing next‐generation DNA sequencing data. Genome Research, 20, 1297– 1303. 10.1101/gr.107524.110 20644199 PMC2928508 · DOI · Paper page
- McPherron, A. C., Lawlert, A. M., & Lee, S.‐J. (1997). Regulation of skeletal muscle mass in mice by a new TGF‐fl superfamily member. Nature, 387, 83– 90. 9139826
- Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B., Gnirke, A., Jaenisch, R., & Lander, E. S. (2008). Genome‐scale DNA methylation maps of pluripotent and differentiated cells. Nature, 454, 766– 770. 18600261 PMC2896277
- Merilä, J., Sheldon, B. C., & Kruuk, L. E. B. (2001). Explaining stasis: Microevolutionary studies in natural populations. In Microevolution Rate, Pattern, Process, Contemporary Issues in Genetics and Evolution (Vol. 8, pp. 199– 222). Springer Science + Business Media. 10.1007/978-94-010-0585-2_13 11838766 · DOI
- Meuwissen, T., Hayes, B., & Goddard, M. (2016). Genomic selection: A paradigm shift in animal breeding. Animal Frontiers, 6, 6– 14. 10.2527/af.2016-0002 · DOI
- Nussey, D. H., Postma, E., Gienapp, P., & Visser, M. E. (2005). Selection on heritable phenotypic plasticity in a wild bird population. Science, 310, 304– 306. 16224020
- Pacis, A., Mailhot‐Léonard, F., Tailleux, L., Randolph, H. E., Yotova, V., Dumaine, A., Grenier, J.‐C., & Barreiro, L. B. (2019). Gene activation precedes DNA demethylation in response to infection in human dendritic cells. Proceedings of the National Academy of Sciences of the United States of America, 116, 6938– 6943. 10.1073/pnas.1814700116 30886108 PMC6452747 · DOI
- Pujol, B., Blanchet, S., Charmantier, A., Danchin, E., Facon, B., Marrot, P., Roux, F., Scotti, I., Teplitsky, C., Thomson, C. E., & Winney, I. (2018). The missing response to selection in the wild. Trends in Ecology & Evolution, 33, 337– 346. 29628266 PMC5937857
- Purcell, S., Neale, B., Todd‐Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., & Sham, P. C. (2007). PLINK: A tool set for whole‐genome association and population‐based linkage analyses. The American Journal of Human Genetics, 81, 559– 575. 10.1086/519795 17701901 PMC1950838 · DOI · Paper page
- Quinlan, A. R., & Hall, I. M. (2010). BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841– 842. 10.1093/bioinformatics/btq033 20110278 PMC2832824 · DOI · Paper page
- Ramakers, J. J. C., Gienapp, P., & Visser, M. E. (2019). Phenological mismatch drives selection on elevation, but not on slope, of breeding time plasticity in a wild songbird. Evolution, 73, 175– 187. 10.1111/evo.13660 30556587 PMC6519030 · DOI
- Rizzoti, K., Brunelli, S., Carmignac, D., Thomas, P. Q., Robinson, I. C., & Lovell‐Badge, R. (2004). SOX3 is required during the formation of the hypothalamo‐pituitary axis. Nature Genetics, 36, 247– 255. 10.1038/ng1309 14981518 · DOI
- Santure, A. W., Gratten, J., Mossman, J. A., Sheldon, B. C., & Slate, J. (2011). Characterisation of the transcriptome of a wild great tit Parus major population by next generation sequencing. BMC Genomics, 12, 283. 10.1186/1471-2164-12-283 21635727 PMC3125266 · DOI
- Santure, A. W., Poissant, J., De Cauwer, I., van Oers, K., Robinson, M. R., Quinn, J. L., Groenen, M. A. M., Visser, M. E., Sheldon, B. C., & Slate, J. (2015). Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations. Molecular Ecology, 24, 6148– 6162. 10.1111/mec.13452 26661500 PMC4738425 · DOI
- Schaper, S. V., Dawson, A., Sharp, P. J., Gienapp, P., Caro, S. P., & Visser, M. E. (2012). Increasing temperature, not mean temperature, is a Cue for avian timing of reproduction. The American Naturalist, 179, E55– E69. 10.1086/663675 22218320 · DOI
- Seisenberger, S., Peat, J. R., Hore, T. A., Santos, F., Dean, W., & Reik, W. (2013). Reprogramming DNA methylation in the mammalian life cycle: Building and breaking epigenetic barriers. Philosophical Transactions of the Royal Society B, 368, 20110330. 10.1098/rstb.2011.0330 PMC3539359 23166394 · DOI
- Sepers, B., Chen, R. S., Memelink, M., Verhoeven, K. J. F., & van Oers, K. (2023). Variation in DNA methylation in avian nestlings is largely determined by genetic effects. Molecular Biology and Evolution, 40, msad086. 10.1093/molbev/msad086 37039566 PMC10139706 · DOI
- Sepers, B., van den Heuvel, K., Lindner, M., Viitaniemi, H., Husby, A., & van Oers, K. (2019). Avian ecological epigenetics: Pitfalls and promises. Journal für Ornithologie, 160, 1183– 1203. 10.1007/s10336-019-01684-5 · DOI
- Shand, J. H., West, D. W., McCartney, R. J., Noble, R. C., & Speake, B. K. (1993). The esterification of cholesterol in the yolk sac membrane of the chick embryo. Lipids, 28, 621– 625. 10.1007/BF02536056 8355590 · DOI
- Shannon, P. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research, 13, 2498– 2504. 10.1101/gr.1239303 14597658 PMC403769 · DOI · Paper page
- Sheldon, B. C., Kruuk, L. E. B., & Merila, J. (2003). Natural selection and inheritance of breeding time and clutch size in the collared flycatcher. Evolution, 57, 406– 420. 10.1111/j.0014-3820.2003.tb00274.x 12683536 · DOI
- Shimada, M., & Yamashita, Y. (2011). The key signaling cascades in granulosa cells during follicular development and ovulation process. Journal of Mammalian Ova Research, 28, 25– 31. 10.1274/jmor.28.25 · DOI
- Skinner, M. K., & Guerrero‐Bosagna, C. (2009). Environmental signals and transgenerational epigenetics. Epigenomics. Epigenomics, 1, 111– 117. 10.2217/epi.09.11 20563319 PMC2886501 · DOI
- Slate, J., Visscher, P. M., MacGregor, S., Stevens, D., Tate, M. L., & Pemberton, J. M. (2002). A genome scan for quantitative trait loci in a wild population of Red Deer (Cervus elaphus). Genetics, 162, 1863– 1873. 12524355 PMC1462362
- Stevenson, T. J., & Prendergast, B. J. (2013). Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proceedings of the National Academy of Sciences of the United States of America, 110, 16651– 16656. 24067648 PMC3799317
- Szeliga, A., Kunicki, M., Maciejewska‐Jeske, M., Rzewuska, N., Kostrzak, A., Meczekalski, B., Bala, G., Smolarczyk, R., & Adashi, E. Y. (2021). The genetic backdrop of hypogonadotropic hypogonadism. International Journal of Molecular Sciences, 22, 13241. 10.3390/ijms222413241 34948037 PMC8708611 · DOI
- Tarka, M., Åkesson, M., Beraldi, D., Hernández‐Sánchez, J., Hasselquist, D., Bensch, S., & Hansson, B. (2010). A strong quantitative trait locus for wing length on chromosome 2 in a wild population of great reed warblers. Proceedings of the Royal Society B, 277, 2361– 2369. 10.1098/rspb.2010.0033 20335216 PMC2894899 · DOI
- van Oers, K., Sepers, B., Sies, W., Gawehns, F., Verhoeven, K. J. F., & Laine, V. N. (2020). Epigenetics of animal personality: DNA methylation cannot explain the heritability of exploratory behavior in a songbird. Integrative and Comparative Biology, 606, 1517– 1530. 10.1093/icb/icaa138 PMC7742756 33031487 · DOI
- Verhagen, I., Gienapp, P., Laine, V. N., Grevenhof, E. M., Mateman, A. C., Oers, K., & Visser, M. E. (2019). Genetic and phenotypic responses to genomic selection for timing of breeding in a wild songbird. Functional Ecology, 33, 1708– 1721. 10.1111/1365-2435.13360 · DOI
- Verhagen, I., Laine, V. N., Mateman, A. C., Pijl, A., de Wit, R., van Lith, B., Kamphuis, W., Viitaniemi, H. M., Williams, T. D., Caro, S. P., Meddle, S. L., Gienapp, P., van Oers, K., & Visser, M. E. (2019). Fine‐tuning of seasonal timing of breeding is regulated downstream in the underlying neuro‐endocrine system in a small songbird. The Journal of Experimental Biology, 222, jeb202481. 10.1242/jeb.202481 31371403 · DOI
- Verhagen, I., Tomotani, B. M., Gienapp, P., & Visser, M. E. (2020). Temperature has a causal and plastic effect on timing of breeding in a small songbird. The Journal of Experimental Biology, 223, jeb218784. 10.1242/jeb.218784 32205357 · DOI
- Viitaniemi, H. M., Verhagen, I., Visser, M. E., Honkela, A., van Oers, K., & Husby, A. (2019). Seasonal variation in genome‐wide DNA methylation patterns and the onset of seasonal timing of reproduction in great tits. Genome Biology and Evolution, 11, 970– 983. 10.1093/gbe/evz044 30840074 PMC6447391 · DOI
- Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M., & Lessells, C. M. (1998). Warmer springs lead to mistimed reproduction in great tits (Parus major). Proceedings of the Royal Society of London B, 265, 1867– 1870. 10.1098/rspb.1998.0514 · DOI
- Wang, S.‐H., Lin, H.‐J., Lin, Y.‐Y., Chen, Y.‐J., Pan, Y.‐H., Tung, C.‐T., Mersmann, H. J., & Ding, S.‐T. (2017). Embryonic cholesterol esterification is regulated by a cyclic AMP‐dependent pathway in yolk sac membrane‐derived endodermal epithelial cells. PLoS One, 12, e0187560. 10.1371/journal.pone.0187560 29161294 PMC5697856 · DOI
- Weiss, J., Meeks, J. J., Hurley, L., Raverot, G., Frassetto, A., & Jameson, J. L. (2003). Sox3 is required for gonadal function, but not sex determination, in males and females. Molecular and Cellular Biology, 23, 8084– 8091. 10.1128/MCB.23.22.8084-8091.2003 14585968 PMC262333 · DOI
- Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer‐Verlag.
- Williams, T. D. (2012). Physiological adaptations for breeding in birds. Princeton University Press.
- Wilson, A. J., Réale, D., Clements, M. N., Morrissey, M. M., Postma, E., Walling, C. A., Kruuk, L. E. B., & Nussey, D. H. (2010). An ecologist's guide to the animal model. Journal of Animal Ecology, 79, 13– 26. 10.1111/j.1365-2656.2009.01639.x 20409158 · DOI
- Wingett, S. W., & Andrews, S. (2018). FastQ screen: A tool for multi‐genome mapping and quality control. F1000Research, 7, 1338. 30254741 PMC6124377
- Zhang, C.‐C., Yuan, W.‐Y., & Zhang, Q.‐F. (2012). RPL1, a gene involved in epigenetic processes regulates phenotypic plasticity in Rice. Molecular Plant, 5, 482– 493. 10.1093/mp/ssr091 22131052 · DOI
- Zhang, Y., Baheti, S., & Sun, Z. (2016). Statistical method evaluation for differentially methylated CpGs in base resolution next‐generation DNA sequencing data. Briefings in Bioinformatics, 19, 374– 386. 10.1093/bib/bbw133 28040747 · DOI
- Zhang, Z., Zhang, L., Wang, B., Wei, R., Wang, Y., Wan, J., Zhang, C., Zhao, L., Zhu, X., Zhang, Y., Chu, C., Guo, Q., Yin, X., & Li, X. (2020). MiR‐337–3p suppresses proliferation of epithelial ovarian cancer by targeting PIK3CA and PIK3CB. Cancer Letters, 469, 54– 67. 10.1016/j.canlet.2019.10.021 31629932 · DOI
Cited by
Sorted by citations
Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives
Majumder, S., Igamberdiev, A. U., & Debnath, S. C. (2025) · Agronomy · doi:10.3390/agronomy15061489 · Cited by 46 · see citing works
- Authors
- Lindner, M., Verhagen, I., Mateman, A. C., van Oers, K., Laine, V. N., & Visser, M. E.
- Affiliations
- University of Groningen (NL)
- Wageningen University & Research (NL)
- Netherlands Institute of Ecology (NL)
- Department of Animal Ecology Netherlands Institute of Ecology (NIOO‐KNAW) Wageningen The Netherlands
- University of Helsinki (FI)
- Corresponding author
- Lindner, Melanie
- Venue
- Evolutionary Applications
- Publisher
- Wiley
- Published
- 2024-06-28
- Volume
- 17
- Issue
- 7
- Pages
- e13703-e13703
- ISSN
- 1752-4563 (ISSN-L)
- 1752-4571
- PMC
- PMC11211926
- OpenAlex
- W4400123532
- Cited by
- 8
- References
- 1
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 1
- FWCI
- 2.12
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Evolutionary Applications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, cc-by)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
- Socio-Environmental Systems Modeling (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Työväentutkimus Vuosikirja (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Funders
- European Research Council (ERC‐2013‐AdG 339092)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- genomic selection, Parus major, DNA methylation, adaptive potential, climate change, hypothalamic-pituitary axis, SOX3, brain development, breeding phenology, myostatin, PIK3CB
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