Sex‐specific fitness effects of unpredictable early life conditions are associated with DNA methylation in the avian glucocorticoid receptor

Abstract

Organisms can adapt to variable environments by using environmental cues to modulate developmental gene expression. In principle, maternal influences can adaptively adjust offspring phenotype when early life and adult environments match, but they may be maladaptive when future environments are not predictable. One of the best-studied 'maternal effects' is through modification of the offspring's hypothalamic-pituitary-adrenal (HPA) axis, the neuroendocrine system that controls responses to stress. In addition to the direct transfer of glucocorticoids from mother to offspring, offspring HPA function and other phenotypes can also be affected by epigenetic modifications like DNA methylation of the glucocorticoid receptor promoter. Here we examine how among-year variation in rainfall is related to DNA methylation during development and fitness in adulthood in the superb starling (Lamprotornis superbus), which lives in a climatically unpredictable environment where early life and adult environments are unlikely to match. We found that DNA methylation in the putative promoter of the glucocorticoid receptor gene is reduced in chicks - particularly in males - born following drier prebreeding periods. Additionally, DNA methylation is lower in males that become breeders than those that never breed. However, there is no relationship in females between DNA methylation and the likelihood of dispersing from the natal group to breed elsewhere. These results suggest that early life conditions may positively affect fitness in a sex-specific manner through chemical modification of an HPA-associated gene. This study is the first to show that epigenetic modifications during early life may influence the fitness of free-living organisms adapted to unpredictable environments.

Differential effects of developmental thermal plasticity across three generations of guppies (Poecilia reticulata): canalization and anticipatory matching

“…There are pronounced differences between males and females in gamete development and their epigenetic state 71 . In starlings, for example, rainfall patterns during early development influenced DNA methylation patterns of glucocorticoid receptor genes in a sex-specific manner, and thereby affected fitness of males and females differentially 72 . Hence, the environment can impact epigenetic profiles of males and females differentially, and thereby cause sex-specific phenotypic trajectories across generations.…”

Dynamic changes in DNA methylation during embryonic and postnatal development of an altricial wild bird

“…Studies of variation in DNA methylation in free-living vertebrates in an ecological context are lacking (Bentz, Sirman, Wada, Navara, & Hood, 2016;Laine et al, 2016; but see Lea et al, 2016;Liebl, Schrey, Richards, & Martin, 2013;Riyahi, Sanchez-Delgado, Calafell, Monk, & Senar, 2015;Viitaniemi et al, 2019), especially during the critical period of development (but see Rubenstein et al, 2016;Sheldon, Schrey, Ragsdale, & Griffith, 2018). Studies of epigenetics in the wild are essential for understanding the fitness consequences of environmentally induced epigenetic modifications, and they could offer valuable insight into the resilience of populations to environmental change.…”

“…To the best of our knowledge, no study has attempted to describe establishment of the methylome in an altricial bird, though methylation has been shown to be sensitive to environmental factors during development (Rubenstein et al, 2016;Sheldon et al, 2018). To the best of our knowledge, no study has attempted to describe establishment of the methylome in an altricial bird, though methylation has been shown to be sensitive to environmental factors during development (Rubenstein et al, 2016;Sheldon et al, 2018).…”

Age‐ and quality‐dependent DNA methylation correlate with melanin‐based coloration in a wild bird

“…In wild animals, there is growing interest in age‐specific DNA methylation (Paoli‐Iseppi et al., 2017), but few studies have examined this and the results are often contradictory. For example, DNA methylation shows age‐specific linear changes in humpback whales ( Megaptera novaeangliae : Polanowski, Robbins, Chandler, & Jarman, 2014) but no changes in superb starlings (Rubenstein et al., 2016), possibly because these studies selected different candidate genes. In black grouse, we found a nonlinear (inverse u‐shaped) pattern of DNA methylation with age, as has similarly been reported in occasional human studies (for an example, see Armstrong, Rakoczy, Rojanathammanee, & Brown‐Borg, 2013).…”

“…There are now a growing number of studies that have examined DNA methylation in wild organisms, mainly in birds (great tits Parus major ; Riyahi, Sánchez‐Delgado, Calafell, Monk, & Senar, 2015; Derks et al., 2016; Laine et al., 2016; Verhulst et al., 2016; eastern blue birds Sialia sialis; Bentz, Sirman, Wada, Navara, & Hood, 2016; red grouse Lagopus lagopus ; Wenzel & Piertney, 2014; house sparrows Passer domesitcus : Liebl, Schrey, Richards, & Martin, 2013; superb starlings Lamprotornis superbus ; Rubenstein et al., 2016). These and other studies have begun to support a role for DNA methylation in mediating ecological effects on phenotypic traits in the wild (e.g., personality and cognition: Laine et al., 2016; Verhulst et al., 2016) and emphasize the dynamic environmental sensitivity of DNA methylation levels across the life course.…”