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Mitochondria as central characters in a complex narrative: Linking genomics, energetics, pace-of-life, and aging in natural populations of garter snakes.
Experimental Gerontology ( IF 3.9 ) Pub Date : 2020-05-06 , DOI: 10.1016/j.exger.2020.110967
Eric J Gangloff 1 , Tonia S Schwartz 2 , Randy Klabacka 3 , Natalie Huebschman 4 , Ang-Yu Liu 5 , Anne M Bronikowski 5
Affiliation  

As a pacesetter for physiological processes, variation in metabolic rate can determine the shape of energetic trade-offs and thereby drive variation in life-history traits. In turn, such variation in metabolic performance and life-histories can have profound consequences for lifespan and lifetime fitness. Thus, the extent to which metabolic rate variation is due to phenotypic plasticity or fixed genetic differences among individuals or populations is likely to be shaped by natural selection. Here, we first present a generalized framework describing the central role of mitochondria in processes linking environmental, genomic, physiological, and aging variation. We then present a test of these relationships in an exemplary system: populations of garter snakes (Thamnophis elegans) exhibiting contrasting life-history strategies - fast-growing, early-reproducing, and fast-aging (FA) versus slow-growing, late-reproducing, and slow-aging (SA). Previous work has characterized divergences in mitochondrial function, reactive oxygen species processing, and whole-organism metabolic rate between these divergent life-history ecotypes. Here, we report new data on cellular respiration and mitochondrial genomics and synthesize these results with previous work. We test hypotheses about the causes and implications of mitochondrial genome variation within this generalized framework. First, we demonstrate that snakes of the FA ecotype increase cellular metabolic rate across their lifespan, while the opposite pattern holds for SA snakes, implying that reduced energetic throughput is associated with a longer life. Second, we show that variants in mitochondrial genomes are segregating across the landscape in a manner suggesting selection on the physiological consequences of this variation in habitats varying in temperature, food availability, and rates of predation. Third, we demonstrate functional variation in whole-organism metabolic rate related to these mitochondrial genome sequence variants. With this synthesis of numerous datasets, we are able to further characterize how variation across levels of biological organization interact within this generalized framework and how this has resulted in the emergence of distinct life-history ecotypes that vary in their rates of aging and lifespan.

中文翻译:

线粒体是复杂叙述中的中心特征:将基因组学,能量学,生活节奏和衰老与吊袜带蛇的自然种群联系起来。

作为生理过程的先驱,新陈代谢率的变化可以确定能量权衡的形状,从而驱动生命历史特征的变化。反过来,新陈代谢表现和生活史的这种变化可能会对寿命和寿命产生深远影响。因此,由于个体或群体之间的表型可塑性或固定的遗传差异而导致的代谢率变化的程度可能由自然选择决定。在这里,我们首先提出一个广义的框架,描述线粒体在连接环境,基因组,生理和衰老变异的过程中的核心作用。然后,我们在一个示例性系统中提出了对这些关系的测试:袜带蛇(Thamnophis elegans)种群表现出截然不同的生活史策略-快速增长,早期繁殖和快速老化(FA)与缓慢生长,晚期繁殖和缓慢老化(SA)。先前的工作描述了这些不同的生活史生态型之间的线粒体功能,活性氧处理和全生物代谢率之间的差异。在这里,我们报告有关细胞呼吸和线粒体基因组学的新数据,并将这些结果与以前的工作进行综合。我们在这种广义框架内测试关于线粒体基因组变异的原因和含义的假设。首先,我们证明了FA生态型的蛇在其整个生命周期中均会提高细胞代谢率,而SA蛇则相反,这表明降低的能量通量与更长的寿命有关。第二,我们发现线粒体基因组中的变异以某种方式建议在整个景观中隔离,这些方式建议根据温度,食物可得性和捕食率的变化对栖息地这种变异的生理后果进行选择。第三,我们证明了与这些线粒体基因组序列变异有关的全生物代谢率的功能变异。通过众多数据集的综合,我们能够进一步表征生物组织各个层面上的变异如何在此通用框架内相互作用,以及这如何导致出现了不同的生命历史生态型,这些生态型的衰老和寿命发生变化。我们证明了与这些线粒体基因组序列变异有关的全生物代谢率的功能变异。通过众多数据集的综合,我们能够进一步表征生物组织各个层面上的变异如何在此通用框架内相互作用,以及这如何导致出现了不同的生命历史生态型,这些生态型的衰老和寿命发生变化。我们证明了与这些线粒体基因组序列变异相关的全生物代谢率的功能变异。通过众多数据集的综合,我们能够进一步表征生物组织各个层面上的变异如何在此通用框架内相互作用,以及这如何导致出现了不同的生命历史生态型,这些生态型的衰老和寿命发生变化。
更新日期:2020-05-06
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