季节性热带干旱森林中野生卷尾猴不同繁殖状态下的活动预算、肠道微生物群稳定性及灵活性
Activity budget and gut microbiota stability and flexibility across reproductive states in wild capuchin monkeys in a seasonal tropical dry forest.
作者信息
Webb Shasta E, Orkin Joseph D, Williamson Rachel E, Melin Amanda D
机构信息
Department of Anthropology and Archaeology, University of Calgary, 2500 University Dr NW, Calgary, AB, T2N 1N4, Canada.
Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA.
出版信息
Anim Microbiome. 2023 Dec 15;5(1):63. doi: 10.1186/s42523-023-00280-6.
BACKGROUND
Energy demands associated with pregnancy and lactation are significant forces in mammalian evolution. To mitigate increased energy costs associated with reproduction, female mammals have evolved behavioural and physiological responses. Some species alter activity to conserve energy during pregnancy and lactation, while others experience changes in metabolism and fat deposition. Restructuring of gut microbiota with shifting reproductive states may also help females increase the energy gained from foods, especially during pregnancy. The goal of this study was to examine the relationships among behaviour, gut microbiota composition, and reproductive state in a wild, non-human primate to better understand reproductive ecology. We combined life history data with > 13,000 behavioural scans and 298 fecal samples collected longitudinally across multiple years from 33 white-faced capuchin monkey (Cebus imitator) females. We sequenced the V4 region of the 16S rRNA gene and used the DADA2 pipeline to analyze microbial diversity. We used PICRUSt2 to assess putative functions.
RESULTS
Reproductive state explained some variation in activity, but overall resting behaviours were relatively stable across pregnancy and lactation. Foraging was less frequent among females in the early stage of nursing compared to the cycling stage, though otherwise remained at comparable levels. Maximum temperature was a strong, significantly positive predictor of resting, while social dominance had a small but significantly negative effect on resting. Ecological variables such as available fruit biomass and rainfall had a small but significantly positive effects on measures of foraging time. Gut microbial community structure, including richness, alpha diversity, and beta diversity remained stable across the reproductive cycle. In pairwise comparisons, pregnant females exhibited increased relative abundances of multiple microbial ASVs, suggesting small changes in relation to reproductive state. Reproductive state was not linked to differential abundance of putative metabolic pathways.
CONCLUSIONS
Previous data suggest that activity budget and the gut microbiome shifts considerably during reproduction. The present study finds that both activity and gut microbial communities are less associated with reproduction compared to other predictors, including ecological contexts. This suggests that behavioural flexibility and gut microbial community plasticity is contrained by ecological factors in this population. These data contribute to a broader understanding of plasticity and stability in response to physiological shifts associated with mammalian reproduction.
背景
与怀孕和哺乳相关的能量需求是哺乳动物进化中的重要驱动力。为了减轻与繁殖相关的能量成本增加,雌性哺乳动物进化出了行为和生理反应。一些物种在怀孕和哺乳期间改变活动以保存能量,而其他物种则经历新陈代谢和脂肪沉积的变化。随着生殖状态的改变而对肠道微生物群进行重组也可能有助于雌性增加从食物中获取的能量,尤其是在怀孕期间。本研究的目的是研究一种野生非人类灵长类动物的行为、肠道微生物群组成和生殖状态之间的关系,以更好地理解生殖生态学。我们将生活史数据与超过13000次行为扫描以及从33只白面卷尾猴(Cebus imitator)雌性个体多年纵向收集的298份粪便样本相结合。我们对16S rRNA基因的V4区域进行了测序,并使用DADA2管道分析微生物多样性。我们使用PICRUSt2评估推定功能。
结果
生殖状态解释了活动的一些变化,但总体而言,在怀孕和哺乳期间休息行为相对稳定。与发情期相比,哺乳期早期雌性的觅食频率较低,不过在其他方面仍处于相当水平。最高温度是休息的一个强烈且显著的正向预测因子,而社会优势地位对休息有微小但显著的负面影响。诸如可获得的果实生物量和降雨量等生态变量对觅食时间的测量有微小但显著的正向影响。肠道微生物群落结构,包括丰富度、α多样性和β多样性在整个生殖周期中保持稳定。在成对比较中,怀孕雌性表现出多种微生物ASV的相对丰度增加,表明与生殖状态存在微小变化。生殖状态与推定代谢途径的差异丰度无关。
结论
先前的数据表明,在繁殖过程中活动预算和肠道微生物群会发生相当大的变化。本研究发现,与包括生态环境在内的其他预测因子相比,活动和肠道微生物群落与繁殖的关联较小。这表明该种群的行为灵活性和肠道微生物群落可塑性受到生态因素的限制。这些数据有助于更广泛地理解对与哺乳动物繁殖相关的生理变化的可塑性和稳定性。
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