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The roles of balancing selection and recombination in the evolution of rattlesnake venom
Nature Ecology & Evolution ( IF 16.8 ) Pub Date : 2022-07-18 , DOI: 10.1038/s41559-022-01829-5
Drew R Schield 1, 2 , Blair W Perry 1, 3 , Richard H Adams 4 , Matthew L Holding 5 , Zachary L Nikolakis 1 , Siddharth S Gopalan 1 , Cara F Smith 6 , Joshua M Parker 7 , Jesse M Meik 8 , Michael DeGiorgio 9 , Stephen P Mackessy 6 , Todd A Castoe 1
Affiliation  

The origin of snake venom involved duplication and recruitment of non-venom genes into venom systems. Several studies have predicted that directional positive selection has governed this process. Venom composition varies substantially across snake species and venom phenotypes are locally adapted to prey, leading to coevolutionary interactions between predator and prey. Venom origins and contemporary snake venom evolution may therefore be driven by fundamentally different selection regimes, yet investigations of population-level patterns of selection have been limited. Here, we use whole-genome data from 68 rattlesnakes to test hypotheses about the factors that drive genomic diversity and differentiation in major venom gene regions. We show that selection has resulted in long-term maintenance of genetic diversity within and between species in multiple venom gene families. Our findings are inconsistent with a dominant role of directional positive selection and instead support a role of long-term balancing selection in shaping venom evolution. We also detect rapid decay of linkage disequilibrium due to high recombination rates in venom regions, suggesting that venom genes have reduced selective interference with nearby loci, including other venom paralogues. Our results provide an example of long-term balancing selection that drives trans-species polymorphism and help to explain how snake venom keeps pace with prey resistance.



中文翻译:

平衡选择和重组在响尾蛇毒液进化中的作用

蛇毒的起源涉及非毒液基因的复制和招募到毒液系统中。一些研究预测定向正选择控制了这一过程。不同蛇种的毒液成分差异很大,并且毒液表型局部适应猎物,导致捕食者和猎物之间的共同进化相互作用。因此,毒液起源和当代蛇毒进化可能是由根本不同的选择机制驱动的,但对种群水平选择模式的研究仍然有限。在这里,我们使用 68 条响尾蛇的全基因组数据来检验有关驱动主要毒液基因区域基因组多样性和分化的因素的假设。我们表明,选择导致了多个毒液基因家族中物种内部和物种之间遗传多样性的长期维持。我们的研究结果与定向正选择的主导作用不一致,而是支持长期平衡选择在塑造毒液进化中的作用。我们还检测到由于毒液区域的高重组率导致连锁不平衡的快速衰减,这表明毒液基因减少了对附近基因座(包括其他毒液旁系同源物)的选择性干扰。我们的结果提供了一个驱动跨物种多态性的长期平衡选择的例子,并有助于解释蛇毒如何与猎物抵抗力保持同步。

更新日期:2022-07-19
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