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    • TPMPA In breeding season small mammals increase dispersal an

    2021-09-17

    In breeding season, small mammals increase dispersal and social communication to maximize their opportunity to mate. In the present study, we found that gerbils in April showed more locomotion and exploratory behavior in the open field test. Moreover, subadult gerbils in April and July were more likely to investigate novel objects than those in September. These characteristics, including novelty-preference and risk-taking in subadults, may promote their communication with potential mates (Somerville, 2013; Spear, 2000). However, adult gerbils in September were more likely to investigate familiar objects, suggesting that they gradually developed a better recognition memory in anticipation of hoarding season. This was supported by previous studies, which show that TPMPA and small mammals have better memory in hoarding season than in other seasons (Barnea and Nottebohm, 1996; LaDage et al., 2010). These seasonal variations in social behavior and recognition memory may facilitate seasonal life-history traits of breeding and food hoarding. GnRH is a critical internal signal from the hypothalamus that regulates reproductive function in all mammalian species (Herbison, 2006). As predicted, GnRH expression in gerbils increased during breeding season compared to hoarding season. Interestingly, the highest level of GnRH was found in April instead of July. Gerbils captured in April are mostly individuals born in early spring or over winter. Studies show that previous harsh experience may promote the onset of reproduction (Wingfield, 1994). Therefore, the highest expression of GnRH would be crucial to trigger the firing of breeding in early spring. In addition, we found that food-induced hoarding gerbils decreased GnRH expression compared to non-hoarding gerbils even in breeding season. Based on our present and previous observation of the video in the field, the gerbils would continuously hoard all the supplemental seeds once one individual in the family found them. In addition to differences in hoarding behavior, the two groups also differed in the amount of food. As the food was necessary to induce hoarding behavior, we cannot find an alternate way to control for this variable. Therefore, we cannot exclude the possibility that differences in the amount of food may attribute, directly or indirectly, to the observed differences in GnRH expression. Our laboratory study showed that the activity increased during hoarding tests, and daily energy expenditure decreased after hoarding tests in the high-hoarding gerbils compared to non-hoarding gerbils, suggesting that the animals would suppress some processes to compensate for the cost of food hoarding (Unpublished data). These data imply that the energy investment for food hoarding may tradeoff with energy investment for reproduction in favor of processes necessary for individual survival. Metabolic fuel hypothesis explores the mechanism of infertility seen in many situations such as famine, cold exposure and excessive exercise on the neuroendocrine perspective (Wade and Jones, 2004). Changes of glycogen and fatty acids can be perceived by some special cell groups in the posterior polar region of the brain, and the activity of GnRH neurons is suppressed through the forebrain when the body is in negative energy balance (Wade et al., 1996; Wade and Jones, 2004). In addition, stress-induced infertility has been confirmed (Ferin, 1999; Whirledge and Cidlowski, 2017). For example, the rats with restraint stress up-regulate the expression of RFamid-related peptide (RFRP), which is the upstream inhibitory transmitter of GnRH neurons (Kirby et al., 2009). The stress in the process of hoarding food of gerbils may affect their breeding. This recession of fertility in hoarding season may be a result of evolution that ensures that the hoarding process runs smoothly for winter survival. Seasonal brain plasticity is a fundamental feature in birds and small mammals that inhabit seasonal environments (Tramontin and Brenowitz, 2000). Activation of adult-born neurons may contribute to recognition memory and adaptation to changing environments (Kempermann et al., 2004). New cells have been documented in several brain regions, including SVZ/OB, DG (Cameron and Mckay, 2001; Lledo and Saghatelyan, 2005), and other non-traditional neurogenic niches, such as the hypothalamus (Lee et al., 2012; Pencea et al., 2001; Kokoeva et al., 2005). Likewise, cell proliferation was also labeled in these brain regions of gerbils. Moreover, the level of cell proliferation in gerbils was higher in breeding season than in the anestrus period. Similar variation is also found in previous studies of ewes, which show that the number of new cells in hypothalamus doubles during the breeding season (Migaud et al., 2011). However, some studies in meadow voles (Microtus pennsylvanicus) show inconsistent results in which the cell proliferation in the hippocampus is suppressed during breeding season (Galea and Mcewen, 1999; Spritzer et al., 2017). Alternatively, the survival of new cells, rather than the proliferation, is influenced by reproductive status in adult male meadow voles (Ormerod and Galea, 2003). These controversial data may reflect species-specific and brain region-specific responses to different seasons. Interestingly, the seasonal difference of cell proliferation in the DG area became undetectable in adults. Many previous studies in rats, Siberian chipmunks (Tamias sibiricus) and black-capped chickadees (Poecile atricapillus) have shown that the adult hippocampal cell proliferation increases in hoarding season in comparison to other seasons (Barnea and Nottebohm, 1994; Pan et al., 2013). The hoarding season for Mongolian gerbils is from September to the end of October. The gerbils have just started to take part in hoarding food when they were captured. This may be the reason why we did not find increased cell proliferation in the hippocampus in September compared to other seasons. The laboratory study shows that high-hoarding gerbils have more cell proliferation in the hippocampus and hypothalamus than non-hoarding gerbils (Unpublished data). Taken together, these data demonstrate that seasonal plasticity of cell proliferation in the adult brain may be involved in mediating seasonal breeding and food hoarding.