Circannual breeding and methylation are impacted by the equinox in Peromyscus

Photoperiod is the major regulator of circannual patterns in mammals, but at animal facilities, despite the controlled conditions, some rodents still exhibit seasonality in their breeding. By evaluating more than 97,000 breeding records of closed Peromyscus colonies, we explored if seasonal breeding patterns exist in animals maintained for several decades at controlled environments.

Seasonal preferences for offspring production were recorded that depended on maternal birth month. Birth in March and September, especially of mothers, showed best fit in 12-knots generalized additive models, implying that the memory of birth month is more intensively carried during the Spring and Autumn equinoxes. The memory of birth month was associated with circannual CpG methylation at birth and revealed that most intense differential methylation, primarily demethylation, occurs in animals that were born in September. Comparison of breeding performance in the periods between the equinoxes showed preference for summer littering by the winter-born animals, especially in the polygamous P. maniculatus bairdii and P. leucopus stocks, and at least in the former species, this was associated with longer estrus cycles. Genes associated with differentially methylated CpGs in winter and summer periods in polygamous species pointed to regulation of gonadotropin hormone releasing hormone secretion. Birth at individually ventilated cages disrupted methylation profiles.

The cyclicity of breeding and methylation patterns suggest that signals other than the photoperiod regulate circannual patterns in deer mice, that reset in the equinox especially in autumn, and that the females are more sensitive to these signals than males.