Transitions in paternal social status predict patterns of offspring growth and metabolic transcription

Abstract

One type of parental effect occurs when changes in parental phenotype or environment trigger changes to offspring phenotype. Such nongenetic parental effects can be precisely triggered in response to an environmental cue in time‐locked fashion, or in other cases, persist for multiple generations after the cue has been removed, suggesting multiple timescales of action. For parental effects to serve as reliable signals of current environmental conditions, they should be reversible, such that when cues change, offspring phenotypes change in accordance. Social hierarchy is a prevalent feature of the environment, and current parental social status could signal the environment in which offspring will be born. Here, we sought to address parental effects of social status and their timescale of action in mice. We show that territorial competition in seminatural environments affects offspring growth. Although dominant males are not heavier than nondominant or control males, they produce faster growing offspring, particularly sons. The timing, effect‐size, and sex‐specificity of this association are modulated by maternal social experience. We show that a change in paternal social status is sufficient to modulate offspring weight: from one breeding cycle to the next, status‐ascending males produce heavier sons than before, and status‐descending males produce lighter sons than before. Current paternal status is also highly predictive of liver transcription in sons, including molecular pathways controlling oxidative phosphorylation and iron metabolism. These results are consistent with a parental effect of social experience, although alternative explanations are considered. In summary, changes in paternal social status are associated with changes in offspring growth and metabolism.

Age-associated epigenetic changes in mammalian sperm: implications for offspring health and development

“…Age-dependent changes in sperm epigenome may be a part of normal developmental program shaped by natural selection to inform better fitness of offspring phenotypes. One recent study demonstrated that paternal dominance status determines the growth rate in offspring in mice, where offspring of dominant males grow faster than the offspring of subordinate fathers even if available food resources are the same ( Cauceglia et al , 2020 ). One interpretation of this intriguing finding is that in nature, dominance usually ensures better access to resources and may increase the fitness of faster-growing offspring.…”

Horizontal transmission of a murine retrovirus is driven by males within semi‐natural enclosures

“…Descriptions of enclosure, including additional photographs, and established/maintenance methods have been provided elsewhere in more detail (e.g. Cauceglia et al., 2020; Gaukler et al., 2015, 2016; Ruff et al., 2013, 2015). Within enclosures, populations are founded by 24–30 mice (16–20 females; 8–10 males); this asymmetric sex ratio is standard for this system and the increased number of females increases the opportunity for vertical transmission.…”

Genetically identical mice express alternative reproductive tactics depending on social conditions in the field

“…Experimental populations of inbred mouse strains (Mus musculus domesticus) living in semi-natural enclosures provide the ideal opportunity for studying the causal impact of social environment on individual competitive and reproductive behaviours. Wild and laboratory mice establish and defend territories when given the space to do so, and territories allow males to monopolize or nearly monopolize access to food and mates [29][30][31][32][33][34][35][36][37]. And the identical genetics and standardized rearing conditions of inbred strains represent an extreme uniformity across individuals as compared with wild populations, allowing us to manipulate a single aspect of animals' social environments and draw causal conclusions about the impact of this manipulation [28].…”