Natural epigenetic variation in bats and its role in evolution

Abstract

When facing the challenges of environmental change, such as habitat fragmentation, organisms have to adjust their phenotype to adapt to various environmental stresses. Recent studies show that epigenetic modifications could mediate environmentally induced phenotypic variation, and this epigenetic variance could be inherited by future generations, indicating that epigenetic processes have potential evolutionary effects. Bats living in diverse environments show geographic variations in phenotype, and the females usually have natal philopatry, presenting an opportunity to explore how environments shape epigenetic marks on the genome and the evolutionary potential of epigenetic variance in bat populations for adaptation. We have explored the natural epigenetic diversity and structure of female populations of the great roundleaf bat (Hipposideros armiger), the least horseshoe bat (Rhinolophus pusillus) and the eastern bent-winged bat (Miniopterus fuliginosus) using a methylation-sensitive amplified polymorphism technique. We have also estimated the effects of genetic variance and ecological variables on epigenetic diversification. All three bat species have a low level of genomic DNA methylation and extensive epigenetic diversity that exceeds the corresponding genetic variance. DNA sequence divergence, epigenetic drift and environmental variables contribute to the epigenetic diversities of each species. Environmentinduced epigenetic variation may be inherited as a result of both mitosis and meiosis, and their potential roles in evolution for bat populations are also discussed in this review. KEY WORDS: DNA methylation, Chiroptera, Mammals, Environmental adaptation IntroductionWhen facing challenges from environmental changes or stresses, organisms have to adapt to the changed environment by genetic mechanisms, physiological adaptability, phenotypic plasticity or moving to a new, more suitable area. The genetic changes may support abundant phenotypic variation in organisms for environmental adaptation, but they occur slowly and cannot keep pace with the rapidly changing environment (Bonduriansky et al., 2012). Recent studies have suggested that epigenetic modifications in eukaryotes could affect genetic expression and thus may mediate phenotypical variation in response to rapid and unpredictable environmental changes without genetic divergence (Dolinoy et al., 2007;Gao et al., 2010; Kucharski et al., 2008). These environmentally induced epigenetic patterns may even be stably inherited by future generations (Grant-Downton and Dickinson, 2006; Jablonka and Lamb, 1998;Richards, 2006), which provides an additional pathway for environmental adaptation and produces a challenge to the Modern Evolutionary Synthesis (Bossdorf et al., 2008; Jablonka and Lamb, 1995; Jablonka et al., 2005), in that the epigenetic process is another source of random variation in natural populations in addition to genetic variance (Massicotte et al., 2011;Schmitz et al., 2011).DNA methylation, one of the key epigenetic markers, is a covalen...

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“…Although, interesting insights regarding the effects of DNA methylation to plasticity and adaptation come from exploring natural populations ( Liu et al. 2015 ; Smith et al.…”

Ancestral and offspring nutrition interact to affect life-history traits inDrosophila melanogaster

“…For example, diversity in the location of methylation marks among populations of bat species may allow them to rapidly buffer changes in crowdedness, meteorological conditions (e.g. temperature), noise and light disturbances [6]. In a second example, early-life grooming of & 2019 The Author(s) Published by the Royal Society.…”

Ancestral and offspring nutrition interact to affect life history traits inDrosophila melanogaster

“…While a substantial portion of 46 effort is directed at piecing together mechanisms of epigenetic gene regulation, biologists have 47 also re-considered the ecological and evolutionary implications of transgenerational effects, by 48 considering the relationship between epigenetic variation and fitness in natural populations 49 (Kilvitis et al, 2014) and how the timing at which a transgenerational effect occurs may 50 determine whether an epigenetic effect is functional versus an impairment (Kuzawa and Thayer, 51 2011). For example, diversity in the location of methylation marks among populations of bat 52 species may allow them to rapidly buffer change in crowdedness, meteorological conditions 53 (e.g., temperature), noise and light disturbances (Liu et al, 2015). In a second example, early-life 54 grooming of rat pups is associated with changes in methylation of HPA-axis related genes, which 55 are associated with low corticosterone levels and lowered anxiety (Zhang and Meaney, 2010).…”