Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: insights from clonal, invasive, polyploid, and domesticated animals

Abstract

There is increasing evidence, particularly from plants, that epigenetic mechanisms can contribute to environmental adaptation and evolution. The present article provides an overview on this topic for animals and highlights the special suitability of clonal, invasive, hybrid, polyploid, and domesticated species for environmental and evolutionary epigenetics. Laboratory and field studies with asexually reproducing animals have shown that epigenetically diverse phenotypes can be produced from the same genome either by developmental stochasticity or environmental induction. The analysis of invasions revealed that epigenetic phenotype variation may help to overcome genetic barriers typically associated with invasions such as bottlenecks and inbreeding. Research with hybrids and polyploids established that epigenetic mechanisms are involved in consolidation of speciation by contributing to reproductive isolation and restructuring of the genome in the neo-species. Epigenetic mechanisms may even have the potential to trigger speciation but evidence is still meager. The comparison of domesticated animals and their wild ancestors demonstrated heritability and selectability of phenotype modulating DNA methylation patterns. Hypotheses, model predictions, and empirical results are presented to explain how epigenetic phenotype variation could facilitate adaptation and speciation. Clonal laboratory lineages, monoclonal invaders, and adaptive radiations of different evolutionary age seem particularly suitable to empirically test the proposed ideas. A respective research agenda is presented.

Keywords: adaptation; epigenetic variation; general-purpose genotype; genome reconfiguration; monoclonal invaders; speciation.

Figure 1

Stochastic developmental and environmentally induced phenotype variation exemplified by genetically identical populations. (A) In a given environment, developmental stochasticity produces a range of epigenetically diverse phenotypes around a mean phenotype (MP). The MP is thought to express an optimal epigenetic profile resulting from the interaction of the genome and the prevailing environment. The range around the MP can be symmetric or asymmetric. In a stable environment the MP holds its position on the scale of possible phenotypes throughout the following generations but the stochastically produced ranges of phenotypes around it may vary to some degree. (B) Different environments induce shifts of the MP on the scale of possible phenotypes. Environmental cues may also have an influence on the range of SPV around the MP

Figure 2

Relationship of genetic and epigenetic diversity in invasive house sparrow, Passer domesticus, from seven Kenyan cities. House sparrows were introduced to Mombasa in the 1950s and have considerably expanded their range since then. Epigenetic diversity was determined by MS-AFLP and genetic diversity by microsatellite analysis. The graph shows that epigenetic diversity is negatively correlated with genetic diversity, suggesting that epigenetic variation may compensate for low genetic variation. h, haplotype diversity; Ho, heterozygosity (redrawn after [60]; photograph by Andreas Mrowetz)

Figure 3

Environmental effects on epigenetic variation in asexual fish Chrosomus eos–neogaeus under natural and experimental conditions. Environmental and genetic joint effect is separated from the pure environmental effect. Epigenetic differences were determined by MS-ALFP and genetic differences by microsatellite analysis. LR1 to ET4 refer to distinct hybrid lineages from the Laurentians region (LR) and Eastern Townships (ET) of southern Quebec (Canada). LR1 lineages are from environmentally stable lakes whereas ET1–ET4 are from environmentally unstable streams. Experimental animals were sampled as larvae from the indicated sites and raised in common garden experiments for five months until adults. P-values refer to significance of the proportion of epigenetic variation explained uniquely by environment. The graph shows differences of environmental effects on epigenetic variation between predictable (LR1) and unpredictable environments (ET1–ET4) and among lineages even if they occur in sympatry (ET3 and ET4). Comparison of LR1 and ET2 in the field and laboratory suggests rapid epigenetic response to environmental change (redrawn after [5]; photograph from [5])

Figure 4

Alteration of fitness traits, DNA content, and DNA methylation level in crayfish after saltational speciation. (A) Marbled crayfish Procambarus virginalis originated from slough crayfish P. fallax by autotriploidization and concomitant change of the sexual system from gonochorism to parthenogenesis. (B) Marbled crayfish (Pv) grow considerably bigger and are more fecund than slough crayfish (Pf). Dots and horizontal bars indicate means and ranges, and figures in brackets give numbers of specimens investigated. (C) Marbled crayfish have a 1.4-fold DNA content in blood cells when compared with the parent species. Vertical bars are SDs of three samples measured by flow cytometry. (D) Global DNA methylation of abdominal musculature and hepatopancreas (major organ of metabolism) is about 20% lower in marbled crayfish than in slough crayfish, suggesting marked alterations of DNA methylation during speciation. Vertical bars are SDs of three samples measured by mass spectrometry (redrawn after [76]; photographs by Chris Lukhaup)

Figure 5

Changes in DNA methylation profiles after hybridization of Xenopus frogs. The graph shows methylated (blue) and unmethylated (red) fragments obtained by MS-AFLP from muscle tissue of parents and their F1 hybrids. Hybrids have higher proportions of methylated fragments than the parental species. Seventy-six methylated fragments are diagnostic of hybrids only suggesting the involvement of DNA methylation in genome reconfiguration after hybridization. Some of the methylated fragments in hybrids are sex-specific and may account for the difference in fertility between females and males (redrawn after [85]; photograph of X. laevis by Benedikt Rauscher, photograph of X. muelleri by Martin Grimm)

Figure 6

Correlation of genetic and epigenetic changes with phylogenetic distance in five species of Darwin’s finches. Red numbers on branches are epimutations (DMRs) and blue numbers are genetic mutations (CNVs) for four species compared with a reference species (Geospiza fortis). The phylogram is based on allele length variation at 16 polymorphic microsatellite loci. Photographs show variation in bill size and shape. The graph shows that the number of DMRs increases consistently with phylogenetic distance, whereas the number of CNVs does not (redrawn after [92]; photographs by Jennifer A. H. Koop and Sarah A. Knutie)

Figure 7

Thought experiment on the role of epigenetic phenotype variation in environmental adaptation and evolution. (A) Starting point is the invasion of a new geographical region by a gravid parthenogenetic female and the subsequent release of genetically uniform but epigenetically and phenotypically diverse progeny (P1–P10). The diversity of the offspring was produced by SPV under the conditions of the old environment. (B) The epigenetically different offspring then occupy different habitats (H1–H5) and are now exposed to different environmental cues. (C) In the following generations, different ecotypes (ET1–ET5) evolve by the interplay of EPV and SPV, TEI of evolutionarily relevant epigenetic signatures, and differential selection (DS) on the epigenetically mediated phenotypes. (D) The conversion of epigenetic diversity (ED) into genetic diversity (GD) and the establishment of ecological barriers may finally lead to the origin of new species

Figure 8

Marbled crayfish Procambarus virginalis (Pv) as promising model of environmental and evolutionary epigenetics. (A) Marbled crayfish produce numerous genetically identical offspring by apomictic parthenogenesis. The lecithotrophic offspring are brooded on the maternal pleopods (arrow) until the 3rd juvenile stage. Genome size and global DNA methylation level are in the order of magnitude of humans (photograph from [174]). (B) In Europe, marbled crayfish has invaded more than 20 water bodies including Lake Moosweiher in southern Germany (arrow) (redrawn after [131], updated). (C, D) Marbled crayfish thrive well in both very simple laboratory settings and natural habitats (photographs from [152]). (E) First global DNA methylation measurement revealed a lower level in wild (Lake Moosweiher, PvMo) than in cultured specimen (Petshop, PvP) (data from [76]). (F) Specimens from the Petshop and Heidelberg (PvH) lineages and from Lake Moosweiher and Madagascar (PvMa), which evolved separately for at least 10 generations, show identity of the complete mitochondrial genomes, demonstrating single origin and monoclonality. They differ from their parent species P. fallax by numerous SNPs (vertical bars). bp, base pairs (redrawn after [76]). (G) Monoclonality of cultured (PvL) and wild marbled crayfish is confirmed by nuclear microsatellites PclG-02 and PclG-26. Sexually reproducing P. fallax shows considerable variation in these microsatellites (redrawn after [76])

Figure 9

Invasive American clone of water flea Daphnia pulex in Africa as promising model to study epigenotype, genotype, and phenotype diversification across space and time. (A) Obligately parthenogenetic female carrying ephippium with dormant eggs (arrow) in brood chamber (from [128], photograph by Joachim Mergeay). (B) The American clone invaded Lake Naivasha in Kenya in about 1927. It successively replaced native D. pulex as revealed by microsatellite analysis of dormant eggs from dated sediments since the year 1920. Stippled line shows gradual decrease of genetic diversity over time (bars indicate 95% confidence). (C) The analysis of 12S rRNA genes of dormant eggs from sediments of Lake Naivasha (LN) dated to the years 1925, 1955 and 2003 demonstrates close genetic relationship of the pre-invasive D. pulex to European strains and identity of the invasive clone with a Canadian strain. (D) The invasive clone has meanwhile spread across the cooler regions of Eastern and Southern Africa and replaced the native populations. Arrow indicates Lake Naivasha (graphs modified after [128])