Complementary histological and genomic analyses reveal marked differences in the developmental trajectories of ovaries in Siberian hamsters raised in long‐ and short‐day lengths

Abstract

Siberian hamsters (Phodopus sungorus) delay sexual development when raised in short-day (SD; 10 hr light: 14 hr dark) conditions, which leads to delayed onset of estrous cycles and ovulations as compared to females raised in long-day (LD; 16 hr light: 8 hr dark) conditions. In addition to the absence of pre-ovulatory follicles and corpora lutea, the ovaries of SD-reared Siberian hamsters are characterized by an abundance of hypertrophied granulosa cells (HGCs) that surround atretic oocytes. To determine the age at which the histology of LD and SD ovaries first diverge, including the initial appearance of HGCs in SD conditions, we examined hamster ovaries histologically at 1, 2, 3, 4, 6, 8, 10, and 12 weeks of age. After identifying subtle differences in LD and SD ovarian histology at 4 weeks of age, we searched for differences in ovarian gene expression at 3 and 8 weeks of age, which correspond to the ages when ovarian histology do not differ (3 weeks) versus the earliest age when HGCs were observed (8 weeks). At 3 weeks, only 14 genes were differentially expressed in LD and SD ovaries, whereas 183 genes were differentially expressed at 8 weeks. Overall, our findings demonstrate that ovarian development under SD conditions is not simply arrested at an early stage of LD development, but rather utilizes a developmental path that is distinct from that used in LD ovaries.

Dissociation of Puberty and Adolescent Social Development in a Seasonally Breeding Species

“…Because photoperiod modulated play behavior at P20 and P30, a pubertal mechanism for altered levels of play is doubtful. In addition to delaying puberty, SD-rearing suppresses gonadal function as early as P20 [3,15], raising the possibility of a prepubertal gonadal mechanism.…”

Folliculogenic factors in photoregressed ovaries: Differences in mRNA expression in early compared to late follicle development

“…Tissues were stained with hematoxylin and eosin to differentiate ovarian structures and 5-6 cross sections per animal were quantified. Structures counted included primordial follicles (oocyte segregated from surrounding environment by squamous granulosa cells), primary follicles (one layer of cuboidal granulosa cells), secondary follicles (two or more layers of cuboidal granulosa cells), tertiary/antral follicles (multiple layers of granulosa cells, clear antrum present), hypertrophied granulosa cells (large potentially atretic follicles lacking oocytes and characteristic of ovaries from SD exposed females; e.g., van den Hurk et al, 2002; Park et al, 2014) and corpora lutea.…”

Matrix metalloproteinase inhibition influences aspects of photoperiod stimulated ovarian recrudescence in Siberian hamsters

“…Sections from all groups were stained with hemotoxylin and counterstained with eosin using a standard protocol, and preantral follicles, antral follicles, corpora lutea (CL), and hypertrophied granulosa cells (also called eosinophilic terminal atretic follicles, luteinized atretic follicles, terminology consistent with Park et al, 2014) were counted across 3–6 ovarian cross sections per animal using the criteria described previously (Moffatt-Blue et al, 2006). …”