Epigenetics As a New Avenue for the Role of Inbreeding Depression in Evolutionary Ecology

NEWS AND COMMENTARY

Epigenetic components of inbreeding depression Epigenetics as a new avenue for the role of inbreeding depression in evolutionary ecology

P-O Cheptou and K Donohue

Heredity (2013) 110, 205–206; doi:10.1038/hdy.2012.66; published online 10 October 2012

ecause of its impacts on major life- lation may contribute to inbreeding effects. alone (Kelly and Willis, 2001). Clearly, such a Bhistory traits (for example, mating sys- Such a clear-cut result is new (see however, genetic architecture of inbreeding depression tem, dispersal, aging), inbreeding depression Bie´mont, 2010) and, if generalisable, will does not fit with scenarios of unconditionally has been central in evolutionary biology. enhance our understanding of the genetic deleterious alleles. Instead, the degree to which Inbreeding depression is defined as the causes of inbreeding depression and potentially alleles are deleterious may depend on environ- reduction in fitness caused by increased modify our expectations of how it will evolve. mental conditions. Regulation of gene expres- homozygosity of individuals due to self- This result provides a mechanistic explana- sion through methylation provides a plausible fertilization or biparental inbreeding. The tion for environment-dependent inbreeding explanation for such results. It is worth noting current population-genetics theory of inbreed- depression, which has long been docu- that such epigenetic mechanisms may be ing depression mainly considers it to be the mented by empirical studies (for example, relevant not only for the evolution inbreeding consequence of recessive deleterious alleles Darwin, 1876). Environmental conditions depression but also for the maintenance of arising through mutations, and secondarily affect the magnitude of inbreeding depres- genetic variation in fitness traits in natural as the consequence of overdominant alleles sion (Armbruster and Reed, 2005), which populations (Charlesworth and Willis, 2009). (Charlesworth and Willis 2009). may change the outcome of selection on More fundamentally, these results of In a recent paper, Vergeer et al. (2012) traits such as stability of mixed mating Vergeer et al. (2012) may also change our have provided intriguing results that may system (Cheptou and Mathias, 2001). Until view of the evolutionary consequences of change our understanding of inbreeding now, there has been little theoretical inves- inbreeding depression, typically viewed as a depression and challenge the classical theory tigation of the causes of environment- constraint imposed by unavoidable deleter- of how inbreeding depression evolves. Using dependent inbreeding depression (however, ious mutations. It has been established that a concise experimental design comparing the see Ronce et al., 2009) in the absence of methylation can be regulated by both genetic fitness of selfed offspring relative to that of mechanisms to explain it (see Cheptou and and environmental factors. As a consequence, outbred offspring, the authors showed that Donohue, 2011 for various hypotheses). As we may speculate that inbreeding depression epigenetic modifications have a major impact methylation is known to be modulated in may evolve as a response to positive selection on inbreeding depression in the perennial part by the environment (Bossdorf et al., on alleles regulating genome methylation. plant Scabiosa columbaria. They first showed 2008), the result of Vergeer et al. (2012) Therefore, although inbreeding depression has that inbred individuals had higher levels of provides a convincing mechanism for such typically been considered to be a constraint methylation than outbred individuals. Second, common observations. Specifically, changes on the evolution of life-history traits such as although inbreeding depression was high in in gene-expression regulation may contri- self-fertilisation (Lande and Schemske, 1985), the species S. columbaria,theyshowedthat bute to fitness differences between selfed the result of Vergeer et al. (2012) indicates inbreeding depression was nearly completely and outcrossed progeny, as the environment that inbreeding depression may be evolutio- removed after chemical demethylation treat- modifies gene expression, those fitness differ- narily labile and may evolve jointly with ments (5-azacytidine) of S. columbaria seedlings. ences (that is, inbreeding depression) are also other life-history traits. This observation that gene silencing through likely to be environment-dependent. Such co-evolution will fundamentally methylation is more prevalent in selfed off- These results of Vergeer et al. (2012) also depart from the classical paradigm of purging spring is intriguing, as it suggests that under- shed new light on several empirical results that dynamics. Importantly, the amplitude of the expression of certain genes can cause fitness do not fit with classical theory on inbreeding methylation effect demonstrated by Vergeer reductions, and that underexpression is asso- depression. Models that invoke mutation-selec- et al. (2012) suggests that such epigenetic ciated with homozygosity. Thus, dosage regu- tion balance suggest that loci responsible for regulation may have a strong effect. We need inbreeding depression typically occur at low to reconcile the low effect of purging as Dr P-O Cheptou is at the UMR 5175 CEFE—Centre frequency. In contrast, empirical studies have detected in experimental studies (Byers and d’Ecologie Fonctionnelle et Evolutive (CNRS), France concluded that loci responsible for inbreeding Waller, 1999) in spite of high variation in and K Donohue is at the Department of Biology, Duke University, Durham, NC, USA depression are often at higher frequencies than inbreeding depression (Winn et al.,2011). E-mail: [email protected] can be predicted by mutation-selection balance What has been considered for several decades News and Commentary 206

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