Genetic Analyses of a Seasonal Interval Timer

Abstract

Seasonal clocks (e.g., circannual clocks, seasonal interval timers) permit anticipation of regularly occurring environmental events by timing the onset of seasonal transitions in reproduction, metabolism, and behavior. Implicit in the concept that seasonal clocks reflect adaptations to the local environment is the unexamined assumption that heritable genetic variance exists in the critical features of such clocks, namely, their temporal properties. These experiments quantified the intraspecific variance in, and heritability of, the photorefractoriness interval timer in Siberian hamsters ( Phodopus sungorus), a seasonal clock that provides temporal information to mechanisms that regulate seasonal transitions in body weight. Twenty-seven families consisting of 54 parents and 109 offspring were raised in a long-day photoperiod and transferred as adults to an inhibitory photoperiod (continuous darkness; DD). Weekly body weight measurements permitted specification of the interval of responsiveness to DD, a reflection of the duration of the interval timer, in each individual. Body weights of males and females decreased after exposure to DD, but 3 to 5 months later, somatic recrudescence occurred, indicative of photorefractoriness to DD. The interval timer was approximately 5 weeks longer and twice as variable in females relative to males. Analyses of variance of full siblings revealed an overall intraclass correlation of 0.71 ± 0.04 (0.51 ± 0.10 for male offspring and 0.80 ± 0.06 for female offspring), suggesting a significant family resemblance in the duration of interval timers. Parent-offspring regression analyses yielded an overall heritability estimate of 0.61 ± 0.2; h2 estimates from parent-offspring regression analyses were significant for female offspring (0.91 ± 0.4) but not for male offspring (0.35 ± 0.2), indicating strong additive genetic components for this trait, primarily in females. In nature, individual differences, both within and between sexes, in the timekeeping properties of seasonal interval timers, and a strong heritable basis thereof, would provide ample substrate for selection to rapidly influence seasonal clocks. Balancing selection in environments where the onset of spring conditions varies from year to year could maintain genetic variance in interval timers and yield interval timers tuned to the local environment.