Aggressive behaviours track transitions in seasonal phenotypes of female Siberian hamsters

Abstract

SUMMARY Seasonally breeding animals exhibit profound physiological and behavioural responses to changes in ambient day length (photoperiod), including changes in reproductive function and territorial aggression. Species where aggression persists when gonads are regressed and circulating levels of gonadal hormones are low, such as Siberian hamsters (Phodopus sungorus) and song sparrows (Melospiza melodia), challenge the well-established framework that gonadal hormones are important mediators of aggression. A solution to this apparent paradox is that a season-specific increase in sensitivity to hormones in brain areas associated with aggression offsets low levels of gonadal hormones during periods of reproductive quiescence. To test this hypothesis, we manipulated photoperiod to induce natural fluctuations in seasonal phenotype across multiple stages of the annual reproductive cycle in female Siberian hamsters that display increased aggression during short-day reproductive quiescence, suggesting that behaviour persists independent of gonadal steroids. Females were housed in long “summer” days or short “winter” days for 10, 24 or 30 weeks to capture gonadal regression, transition back to a reproductively functional state and full gonadal recrudescence, respectively. Long-day animals maintained reproductive functionality and displayed low aggression across all time points. By week 10, short-day reproductively responsive females underwent gonadal regression and displayed increased aggression; non-responsive animals showed no such changes. At week 24, animals were in a transitional period and displayed an intermediate phenotype with respect to reproduction and aggression. By week 30, short-day females were fully recrudesced and returned to long-day-like levels of aggression. Consistent with our hypothesis, gonadally regressed females displayed decreases in 17β-oestradiol (oestradiol) levels, but site-specific increases in the abundance of brain oestrogen receptor-alpha (ERα) in regions associated with aggression, but not reproduction. Increased site-specific ERα may function as a compensatory mechanism to allow increased responsiveness to oestradiol in regulating aggression in lieu of high circulating concentrations of hormones. Collectively, these results broaden our understanding of how breeding phenology maps onto social behaviour and the mechanisms that have evolved to coordinate behaviours that occur in non-breeding contexts.

Seasonal patterns of melatonin alter aggressive phenotypes of female Siberian hamsters

“…In addition to a shift in hormonal source, seasonal changes in steroid synthesis and metabolism within target tissues have been reported. For example, heightened steroid metabolism, including increased expression of the enzyme aromatase, which catalyses the conversion of T to E 2 , and elevated sensitivity to hormones (eg, E 2 ), such as increased expression of oestrogen receptors, within discrete brain regions, have been reported as key regulators of aggression in birds, 22,23 mammals, 24‐26 and species that display a sex role reversal in aggression 27,28 . Collectively, these mechanisms are consistent with the hypothesis that seasonal changes in aggression map onto changes in neuroendocrine processes; however, they do not describe, in turn, how aggression influences these processes.…”

“…Throughout the study, hamsters were weighed on a weekly basis to track changes in body mass, and coat colour was assessed to document the transition from summer brown/grey to winter white 47,48 . In addition, oestrous cycles were monitored via vaginal cytology for all experimental animals 5 days prior to behavioural trials to determine whether females were cycling, as described previously 25,47‐49 . Hamsters were characterised as reproductively functional if they had functional reproductive tissues (ie, ovaries and uterine horns), displayed no significant change in body mass (≤ 10%) and maintained a brown/grey coat colour.…”

“…Pre‐ and post‐aggression levels of serum DHEA, T and E 2 were quantified using commercially available enzyme immunoassay kits that have been previously validated in this species (DHEA: assay sensitivity = 0.108 ng mL ‐1 ; ALPCO Diagnostics, Salem, NH, USA; 20‐DHEHU‐E01 39,53 ; T: assay sensitivity = 5.67 pg mL ‐1 ; Assay Design, Ann Arbor, MI, USA; 900‐065 54,55 ; E 2 : assay sensitivity = 14.0 pg mL ‐1 ; Enzo Life Sciences, Farmingdale, NY, USA; ADI‐900‐174 25 ). Each of these kits is highly specific for the hormone of interest and have negligible or undetectable cross‐reactivity with other steroid hormones (DHEA kit: sulfated DHEA = 0.01%, T = 0.01%, E 2 = < 0.01%, cortisol = < 0.01%; T kit: 19‐hydroxytestosterone = 14.6%, androstenedione = 7.2%, DHEA = 0.7%, E 2 = 0.4%; E 2 kit: oestrone = 17.8%, oestriol = 0.9%, T = 0.01%, DHEA = < 0.001%).…”

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

“…Although gonadal steroids are known to promote aggression in numerous species [31], experiments have repeatedly shown that SD-housing increases, and gonadectomy has little to no effect on, aggression in adult male and female Siberian hamsters when tested in the resident-intruder paradigm [32–36]. Instead, adrenal hormones have been proposed to regulate aggression in SD-housed Siberian hamsters [37–39] and several other seasonal species [40].…”

Evolutionary diversity as a catalyst for biological discovery

“…For example, male cichlid fish rapidly transition to dominant physiological and behavioral phenotypes in response to social opportunities; Siberian hamsters ( Phodopus sungorus ) exhibit seasonal variation in aggression; and honeybees ( Apis mellifera ) transition through different social roles in the colony throughout the lifespan (Ben-Shahar, 2005; Maruska & Fernald, 2010; Maruska et al, 2013; Rendon et al, 2017; Robinson, 2002; Wen et al, 2004). These and many other examples suggest that the biological systems modulating social behavior exhibit functional plasticity across developmental, seasonal, and rapid neuromodulatory timescales in a species-specific fashion.…”