Epigenetics and the Evolution of Darwin’s Finches

Skinner, Michael K.; Gurerrero-Bosagna, Carlos; Haque, M. Muksitul; Nilsson, Eric; Koop, Jennifer A. H.; Knutie, Sarah A.; Clayton, Dale H.

doi:10.1093/gbe/evu158

Cited by 108 publications

(120 citation statements)

References 58 publications

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“…In most wild animal populations examined to date, there has been an excess of DNA methylation variation relative to genetic variation (Massicotte et al, 2011;Mor an & P erez-Figueroa, 2011;Liu et al, 2012;Massicotte & Angers, 2012;Schrey et al, 2012;Liebl et al, 2013;Skinner et al, 2014;Wenzel & Piertney, 2014). First investigations into epigenetic variation in wild animal populations involved the salmonid, Oncorhynchus mykiss (Blouin et al, 2010).…”

Section: Population Epigenetics In the Wildmentioning

confidence: 99%

Epigenetics in natural animal populations

Barrett

2017

J of Evolutionary Biology

137

127

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Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally-mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.

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Section: Population Epigenetics In the Wildmentioning

confidence: 99%

Epigenetics in natural animal populations

Barrett

2017

J of Evolutionary Biology

137

127

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“…Recent studies showed that methylation changes significantly contributed to the molecular basis of evolution (17,19). As a heritable epigenetic modification, methylation is believed to change (usually suppress) the transcription of genes by either altering the DNA structure or blocking the binding of transcriptional factors with DNA double-strand (21-24).…”

Section: Methylation Modification Of S Galili P53 As a Results Of Adamentioning

confidence: 99%

“…In addition to gene mutations, heritable epigenetic changes occur more frequently with paramount importance for adaptive evolution (17)(18)(19). We report here that the two contiguous Significance p53 has been shown to play important roles in environmental adaptive evolution.…”

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confidence: 80%

Adaptive methylation regulation ofp53pathway in sympatric speciation of blind mole rats,Spalax

Zhao

Tang

Yang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Epigenetic modifications play significant roles in adaptive evolution. The tumor suppressor p53, well known for controlling cell fate and maintaining genomic stability, is much less known as a master gene in environmental adaptation involving methylation modifications. The blind subterranean mole rat Spalax eherenbergi superspecies in Israel consists of four species that speciated peripatrically. Remarkably, the northern Galilee species Spalax galili (2n = 52) underwent adaptive ecological sympatric speciation, caused by the sharply divergent chalk and basalt ecologies. This was demonstrated by mitochondrial and nuclear genomic evidence. Here we show that the expression patterns of the p53 regulatory pathway diversified between the abutting sympatric populations of S. galili in sharply divergent chalk-basalt ecologies. We identified higher methylation on several sites of the p53 promoter in the population living in chalk soil (chalk population). Site mutagenesis showed that methylation on these sites linked to the transcriptional repression of p53 involving Cut-Like Homeobox 1 (Cux1), paired box 4 (Pax 4), Pax 6, and activator protein 1 (AP-1). Diverse expression levels of p53 between the incipiently sympatrically speciating chalk-basalt abutting populations of S. galili selectively affected cell-cycle arrest but not apoptosis. We hypothesize that methylation modification of p53 has adaptively shifted in supervising its target genes during sympatric speciation of S. galili to cope with the contrasting environmental stresses of the abutting divergent chalk-basalt ecologies.evolution | speciation | ecological stress and adaptation | epigenetics S ympatric speciation without geographic isolation is becoming more convincing with the accumulation of supportive genetic evidence (1-3). As we previously proposed (1, 3), sympatric speciation occurs during the adaptive evolution of the Israeli subterranean blind mole rat Spalax galili (2n = 52) living in the Galilee in northern Israel. Genetic and physiological differences were observed from two abutting populations of S. galili living in sharply divergent soil types (chalk and basalt) including population-specific haplotype mitochondrial (mt) DNA pattern, population-unique SNPs of genome, different activity patterns, and distinct oxygen consumption (1, 3). This is the first demonstration, to our knowledge, of sympatric speciation in subterranean mammals, certainly in the genus Spalax, which usually speciates peripatrically or allopatrically (4).The tumor suppressor gene p53 has been underappreciated for its roles in environmental adaptation. As a sensor of stresses including genotoxic stress and hypoxia (5, 6), p53 is also a master gene of diversity during adaptive evolution (7-11), although this perspective is less studied than its role in cancer suppression. Modifications of p53 in different levels during adaptive evolution confer the animal's selective advantage by regulating adaptive cell fates. Our recent study demonstrated that variation of p53 is important for ada...

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“…Epigenetic modifications can also survive the reprogramming events during fertilization and embryonic development, meaning that the DNA-methylome may be inherited over generations, leading to heritable epigenetic effects with markers that can stay for several generations [108,109]. Adding another layer of complexity to DNA methylation and its effect on genome is the potential mutagenic effects, a potential driver for evolution [110,111].…”

Section: Dna Methylationmentioning

confidence: 99%

“…Finally, CpG methylations are dependent on the genome, and SNP variation has the potential to both allow and deny DNA methylation at specific positions. A study of speciation in Darwin finches suggests that methylation patterns are not only inherited over a few generations, but transgenerationally over millennia and can be as important as genomic mutations [111]. Methylations are also suggested to have modified the genome, adding a new layer of complexity to epigenetic mechanisms, with epimutations moving to the stable realm of the genome [110].…”

Section: Gene Regulation and Domesticationmentioning

confidence: 99%

Chicken domestication : Effects of tameness on brain gene expression and DNA methylation

Bélteky¹

2016

Linköping Studies in Science and Technology. Dissertations

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Domestication greatly increases phenotypic variation in a short time span, with selection for a single phenotype and a plethora of associated phenotypic changes as an outcome of the process. The domestication process influences the underlying genomic architecture of a species, and the success and speed of the process is likely influenced by it. The main aims of my thesis was to study how domestication affects the brain of chickens: specifically changes in morphology, gene expression, and DNA methylation. Differences in gene expression and DNA methylation between White Leghorn and Red Junglefowl chickens were mapped, and inheritance of these patterns were quantified, indicating a faithful transmission of breed-specific epigenetic markers. Selection on the behavioral trait fearfulness, generated high and low fearful lines of Red Junglefowl. Both the parental population and the fifth selected generation were used for the analyses in this thesis. One experiment studied morphological changes in the brain and other vital organs, and found that relative total brain size increased in high fearful birds, as a consequence of an increase in cerebral hemisphere size in high fearful birds and not in low fearful birds. Also, the relative heart, liver, spleen and testis size increased in high fearful birds, indicating correlated morphological changes with selection for fearfulness. Two additional experiments examined differential gene expression in the hypothalamus and the anterior cerebral hemisphere. The hypothalamus differed in expression of genes with reproductive and immunological functions, whilst the cerebral hemisphere differed in expression of genes related to social behaviors and neurological functions especially those upregulated in low fearful birds. These results indicate the occurrence of tissue-and species-specific changes in gene expression as overlap with other domestication events were nearly nonexistent. A fourth experiment sought to associate the change in fear levels and gene expression differences with DNA methylation. Chromosomal regions with differential DNA methylation between high and low fearful birds were identified, and genes in these regions had annotated functions relevant to phenotypic differences between the selection lines. This thesis is the first to study the genetic alterations of domestication using the wild ancestor of an already domesticated species to repeat the domestication process selecting against fear of humans. The findings corroborate results from previous comparisons of wild and domestic animals, and further support the theory that rigorous selection for a behavioral trait can cause a cascade of genetic and epigenetic changes facilitating the domestication of a population. Populärvetenskaplig sammanfattningDomesticering, när en population djur anpassas till ett liv i fångenskap och nära kontakt med människor, är en process som under kort tid ger upphov till stora förändringar hos djuret under selektion, såsom skillnader i beteende, fysiologi, storlek, reproduktion och fä...

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Epigenetics and the Evolution of Darwin’s Finches

Cited by 108 publications

References 58 publications

Epigenetics in natural animal populations

Epigenetics in natural animal populations

Adaptive methylation regulation ofp53pathway in sympatric speciation of blind mole rats,Spalax

Chicken domestication : Effects of tameness on brain gene expression and DNA methylation

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