Data from: Circadian rhythms vary over the growing season and correlate with fitness components

Circadian clocks have evolved independently in all three domains of life, suggesting that internal mechanisms of time-keeping are adaptive in contemporary populations. However, the performance consequences of either discrete or quantitative clock variation have rarely been tested in field settings. Clock sensitivity of diverse segregating lines to the environment remains uncharacterized as do the statistical genetic parameters that determine evolutionary potential. In field studies with Arabidopsis thaliana, we found that major perturbations to circadian cycle length (referred to as clock period) via mutation reduce both survival and fecundity. Subtler adjustments via genomic introgression of naturally occurring alleles indicated that clock periods slightly >24 hrs were adaptive, consistent with prior models describing how well the timing of biological processes is adjusted within a diurnal cycle (referred to as phase). In segregating recombinant inbred lines (RILs), circadian phase varied up to two hours across months of the growing season, and both period and phase expressed significant genetic variances. Performance metrics including developmental rate, size, and fruit set were described by principal components (PC) analyses and circadian parameters correlated with the first PC, such that period lengths slightly >24 hrs were associated with improved performance in multiple RIL sets. These experiments translate functional analyses of clock behavior performed in controlled settings to natural ones, demonstrating that quantitative variation in circadian phase is highly responsive to seasonally variable abiotic factors. The results expand upon prior studies in controlled settings, showing that discrete and quantitative variation in clock phenotypes correlate with performance in nature.

生物钟（circadian clock）在所有三个生命域中均独立演化，这提示内在计时机制在当代种群中具备适应性优势。然而，无论是离散还是量化的生物钟变异，其对生物表现的影响极少在野外环境中得到验证。不同分离品系的生物钟环境敏感性，以及决定进化潜力的统计遗传参数，均未得到解析。在以拟南芥（Arabidopsis thaliana）为材料的野外研究中，我们发现通过突变对生物钟周期长度（即钟周期（clock period））造成的显著扰动，会同时降低植株的存活率与繁殖力。通过对天然存在的等位基因进行基因组渐渗实现的更细微的生物钟调整实验表明，略长于24小时的钟周期具有适应性，这与此前描述生物过程时序在昼夜周期内调控精度的模型相一致——该模型将昼夜周期内生物过程的时序调控状态称为相位（phase）。在分离重组自交系（recombinant inbred lines, RILs）中，生物钟相位在生长季的不同月份间可相差达2小时，且钟周期与相位均存在显著的遗传变异。包括发育速率、植株大小和结实量在内的表现指标可通过主成分（principal components, PC）分析进行整合，且生物钟参数与第一主成分显著相关：在多个重组自交系群体中，略长于24小时的钟周期均与更优的生物表现相关。本研究将受控环境下开展的生物钟行为功能分析拓展至自然环境，证实生物钟相位的量化变异对季节变动的非生物因子具有高度响应性。本研究结果拓展了此前受控环境下的相关研究，证明生物钟表型的离散与量化变异均与野外自然环境中的生物表现显著相关。