Dynamic expressions of hypothalamic genes regulate seasonal breeding in a natural rodent population.

Seasonal breeding is a universal reproductive strategy in many animals. Hypothalamic genes, especially type 2 and 3 iodothyronine deiodinases (Dio2/3), RFamide-related peptide 3 (Rfrp-3), kisspeptin (Kiss-1) and gonadotropin-releasing hormone (GnRH), are involved in a photoperiodic pathway that encodes seasonal signals from day length in many vertebrate species. However, the seasonal expression patterns of these genes in wild mammals are less studied. Here, we present a four-year field investigation to reveal seasonal rhythm and age-dependent reproductive activity in male Brandt's voles (Lasiopodomys brandtii) and to detect relationships among seasonal expression profiles of hypothalamic genes, testicular activity, age and annual day length. From breeding season (April) to nonbreeding season (October), adult male voles displayed a synchronous peak in gonadal activity with annual day length around summer solstice, which was jointly caused by age structure shifts and age-dependent gonadal development patterns. Overwintered males maintained reproductive activity until late in the breeding season, whereas most newborn males terminated gonadal development completely, except for a minority of males born early in spring. Consistently, the synchronous and opposite expression profiles of Dio2/3 suggest their central function to decode photoperiodic signals and to predict the onset of the nonbreeding season. Moreover, changes in Dio2/3 signals may guide the actions of Kiss-1 and Rfrp-3 to regulate the age-dependent divergence of reproductive strategy in wild Brandt's vole. Our results provide evidence on how hypothalamic photoperiod genes regulate seasonal breeding in a natural rodent population.

Kinship analysis reveals reproductive success skewed toward overwintered Brandt's voles in semi-natural enclosures.

Age structure and seasonality influence the population fluctuations of small rodents. Age determines body weight and social experience, while seasonality regulates the duration of the breeding season and onset of sexual maturity in newborn offspring. Therefore, reproductive success and skew usually occur in different age groups. Brandt's vole (Lasiopodomys brandtii) is a social, short-lived and seasonal breeding small rodent with a dramatic seasonal population fluctuation, but reproductive skew is not fully understood in this species. In the present study, we determined kinship in semi-natural enclosure populations using microsatellite markers based on genotyping, analyzed the reproductive skew between sexes and between overwintered and newborn voles, and monitored variation in male reproductive activity by testing fecal testosterone levels throughout the year. Overwintered voles had the most reproductive success along with a striking increase in the population size in the enclosures, with all biological fathers and 77.8% of biological mothers, which had 100% and 87% of the total offspring, respectively. Compared to overwintered voles, reproductive skews were significantly higher in potential overwintered and newborn parents, implying the possible reproductive suppression of newborn voles by dominant overwintered voles. Moreover, both heavier body weight and higher testosterone levels in overwintered males supported their potential social status in the population. Our study provided new evidence for reproductive skew and differentiation of postnatal gonadal development patterns of different age groups in Brandt's vole.