Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
Parallel clinal variation in the mid-day siesta of Drosophila melanogaster implicates continent-specific targets of natural selection.
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DOI：
10.1371/journal.pgen.1007612
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发表时间：
2018-09
期刊：
影响因子：
4.5
通讯作者：
Edery I
中科院分区：
文献类型：
--
作者：
Yang Y;Edery I
与许多白天活动的动物相似，黑腹果蝇的午睡时间随着环境温度的升高而变得更加稳定，这是一种旨在最大限度地减少暴露于热量的适应性反应。午间午睡水平部分地由在生物钟基因周期（per）的3'非翻译区（UTR）中发现的小内含子（称为dmpi 8）的热敏剪接调节。利用研究得很好的D.黑腹果蝇纬度渐变沿着澳大利亚东海岸，我们表明，苍蝇从温带人口睡眠较少，在白天相比，从热带地区。我们在per的3' UTR中鉴定了四个单核苷酸多态性（SNP）的组合，产生几种不同的单倍型。这些单倍型中最丰富的两种表现出相对频率的热带-温带分布。有趣的是，与那些携带温带变体的转基因果蝇相比，具有主要热带同种型的转基因果蝇表现出白天睡眠增加和dmpi 8剪接减少。我们的研究结果强烈表明，对于D.在澳大利亚的黑腹果蝇中，日常睡眠行为的热适应包括对每3' UTR中祖先来源的多态性的空间变化选择，所述多态性差异地控制dmpi 8剪接效率。先前的研究表明，来自高海拔地区的非洲苍蝇表现出中午午睡水平的降低，这表明各大洲平行的纬度和海拔适应。然而，在非洲果蝇中没有观察到每3' UTR单倍型的地理变异，这为自然选择在实现平行适应中针对的因素的洲际变异提供了令人信服的案例。我们认为，能够校准中午午睡水平，以更好地匹配当地的温度范围是一个关键的适应有助于成功的殖民D。生活在撒哈拉以南非洲低地的黑腹动物。在温暖的气候中，包括人类在内的许多动物都会在中午午睡，几乎可以肯定，这是一种将长时间暴露在中午炎热的阳光下的伤害降到最低的行为。但是那些适应了更凉爽更温和的气候的动物呢，它们的午睡会不会不那么明显呢？事实上，我们表明，在常见的果蝇，果蝇黑腹，那些来自澳大利亚温带地区的表现出较少的中午午睡相比，他们的热带同行。先前的研究表明，中午的睡眠水平部分受到一种名为周期（per）的“时钟”基因的调节，除了其他日常节奏外，它还控制着觉醒-睡眠周期的时间。我们确定了几个DNA差异的每一个基因，显示地理变异，并有助于白天睡眠的差异，从热带和温带地区的苍蝇通过一种机制，涉及如何以及温度敏感的内含子在每被删除。以前在适应高海拔较低温度的非洲苍蝇中观察到类似的中午睡眠减少。总之，我们的研究结果提供了一个罕见的例子，纬度和海拔导致类似的行为适应温度。此外，研究结果表明，在用于实现相同的热适应较冷的气候的进化解决方案的洲际差异。
Similar to many diurnal animals, Drosophila melanogaster exhibits a mid-day siesta that is more robust as ambient temperature rises, an adaptive response aimed at minimizing exposure to heat. Mid-day siesta levels are partly regulated by the thermosensitive splicing of a small intron (termed dmpi8) found in the 3’ untranslated region (UTR) of the circadian clock gene period (per). Using the well-studied D. melanogaster latitudinal cline along the eastern coast of Australia, we show that flies from temperate populations sleep less during the day compared to those from tropical regions. We identified combinations of four single nucleotide polymorphisms (SNPs) in the 3’ UTR of per that yield several different haplotypes. The two most abundant of these haplotypes exhibit a reciprocal tropical-temperate distribution in relative frequency. Intriguingly, transgenic flies with the major tropical isoform manifest increased daytime sleep and reduced dmpi8 splicing compared to those carrying the temperate variant. Our results strongly suggest that for a major portion of D. melanogaster in Australia, thermal adaptation of daily sleep behavior included spatially varying selection on ancestrally derived polymorphisms in the per 3’ UTR that differentially control dmpi8 splicing efficiency. Prior work showed that African flies from high altitudes manifest reduced mid-day siesta levels, indicative of parallel latitudinal and altitudinal adaptation across continents. However, geographical variation in per 3’ UTR haplotypes was not observed for African flies, providing a compelling case for inter-continental variation in factors targeted by natural selection in attaining a parallel adaptation. We propose that the ability to calibrate mid-day siesta levels to better match local temperature ranges is a key adaptation contributing to the successful colonization of D. melanogaster beyond its ancestral range in the lowlands of Sub-Saharan Africa. In warm climates many animals, including humans, exhibit a mid-day siesta, almost certainly a behavior meant to minimize the harm from prolonged exposure to the hot mid-day sun. But what about animals that adapted to cooler more temperate climates, might they have a less pronounced siesta? Indeed, we show that in the common fruit fly, Drosophila melanogaster, those from temperate regions in Australia exhibit less mid-day siesta compared to their tropical counterparts. Prior work showed that mid-day sleep levels are partially regulated by a ‘clock’ gene called period (per), which controls the timing of wake-sleep cycles in addition to other daily rhythms. We identified several DNA differences in the per gene that show geographical variation and contribute to the daytime sleep differences in flies from tropical and temperate regions via a mechanism that involves how well a temperature-sensitive intron in per is removed. A similar reduction in mid-day sleep was previously observed in African flies that adapted to the cooler temperatures found at high altitudes. Together, our findings provide a rare example where latitude and altitude lead to a similar behavioral adaptation to temperature. Moreover, the results suggest inter-continental differences in the evolutionary solutions used to attain the same thermal adaptation to cooler climates.
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