Large-effect mutations generate trade-off between predatory and locomotor ability during arms race coevolution with deadly prey.

Large-effect mutations generate trade-off between predatory and locomotor ability during arms race coevolution with deadly prey.
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DOI:
10.1002/evl3.76
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发表时间:
2018-08
期刊:
影响因子:
5
通讯作者:
Brodie ED 3rd
Brodie ED 3rd
中科院分区:
生物学1区
文献类型:
--
作者:
Hague MTJ;Toledo G;Geffeney SL;Hanifin CT;Brodie ED Jr;Brodie ED 3rd

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适应性进化对一个选择性挑战的反应可能会破坏其他重要的性能方面。这种进化权衡预计会出现在局部适应的过程中,但目前尚不清楚这些表型妥协是否是简单氨基酸取代的拮抗作用的结果。我们测试了与在普通束带蛇(Thamnophis sirtalis)骨骼肌中的电压门控钠通道(NaV1.4)中赋予河豚毒素(TTX)抗性的有益突变相关的权衡。加州和太平洋西北部的独立谱系独立地进化出了对NaV1.4孔的TTX抗性变化,这是与有毒猎物Taricha属蝾螈的军备竞赛共同进化的结果。来自加州血统的蛇,与具有祖先TTX敏感通道的个体相比,具有已知赋予毒素抗性大幅增加的等位基因(NaV 1.4LVNV)的纯合子,爬行速度显著降低。天然蛇NaV1.4蛋白的异源表达表明,相同的NaV1.4LVNV等位基因赋予TTX抗性的显著增加和整体通道兴奋性的相关降低。我们的研究结果表明,在军备竞赛共同进化过程中积累并有益地干扰毒素结合的相同突变也会导致通道电生理功能的变化,这可能会影响生物体的表现。这种权衡只在捕食者谱系中是明显的,其中共同进化导致了最极端的抗性表型,由四个关键氨基酸取代决定。如果这些生物物理变化也转化为适应性成本,例如,通过T。sirtalis迅速逃脱捕食者,那么在这个单一的基因座多效性可能有助于观察到的TTX抗性水平的变化在整个马赛克景观的共同进化。
Adaptive evolution in response to one selective challenge may disrupt other important aspects of performance. Such evolutionary trade‐offs are predicted to arise in the process of local adaptation, but it is unclear if these phenotypic compromises result from the antagonistic effects of simple amino acid substitutions. We tested for trade‐offs associated with beneficial mutations that confer tetrodotoxin (TTX) resistance in the voltage‐gated sodium channel (NaV1.4) in skeletal muscle of the common garter snake (Thamnophis sirtalis). Separate lineages in California and the Pacific Northwest independently evolved TTX‐resistant changes to the pore of NaV1.4 as a result of arms race coevolution with toxic prey, newts of the genus Taricha. Snakes from the California lineage that were homozygous for an allele known to confer large increases in toxin resistance (NaV1.4LVNV) had significantly reduced crawl speed compared to individuals with the ancestral TTX‐sensitive channel. Heterologous expression of native snake NaV1.4 proteins demonstrated that the same NaV1.4LVNV allele confers a dramatic increase in TTX resistance and a correlated decrease in overall channel excitability. Our results suggest the same mutations that accumulate during arms race coevolution and beneficially interfere with toxin‐binding also cause changes in electrophysiological function of the channel that may affect organismal performance. This trade‐off was only evident in the predator lineage where coevolution has led to the most extreme resistance phenotype, determined by four critical amino acid substitutions. If these biophysical changes also translate to a fitness cost—for example, through the inability of T. sirtalis to quickly escape predators—then pleiotropy at this single locus could contribute to observed variation in levels of TTX resistance across the mosaic landscape of coevolution.
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