Predator-prey interactions often lead to the coevolution of adaptations associated with avoiding predation and, for predators, overcoming those defences. Antagonistic coevolutionary relationships are often not simple interactions between a single predator and prey but rather a complex web of interactions between multiple coexisting species. Coevolution between venomous rattlesnakes and small mammals has led to physiological venom resistance in several mammalian taxa. In general, viperid venoms contain large quantities of snake venom metalloproteinase toxins (SVMPs), which are inactivated by SVMP inhibitors expressed in resistant mammals. We explored variation in venom chemistry, SVMP expression, and SVMP resistance across four co-distributed species (California Ground Squirrels, Bryant's Woodrats, Southern Pacific Rattlesnakes, and Red Diamond Rattlesnakes) collected from four different populations in Southern California. Our aim was to understand phenotypic and functional variation in venom and venom resistance in order to compare coevolutionary dynamics of a system involving two sympatric predator-prey pairs to past studies that have focused on single pairs. Proteomic analysis of venoms indicated that these rattlesnakes express different phenotypes when in sympatry, with Red Diamonds expressing more typical viperid venom (with a diversity of SVMPs) and Southern Pacifics expressing a more atypical venom with a broader range of non-enzymatic toxins. We also found that although blood sera from both mammals were generally able to inhibit SVMPs from both rattlesnake species, inhibition depended strongly on the snake population, with snakes from one geographic site expressing SVMPs to which few mammals were resistant. Additionally, we found that Red Diamond venom, rather than woodrat resistance, was locally adapted. Our findings highlight the complexity of coevolutionary relationships between multiple predators and prey that exhibit similar offensive and defensive strategies in sympatry.

中文翻译：

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两种同域响尾蛇及其猎物的毒液和毒液抗性的表型和功能变异。

捕食者与猎物的相互作用通常会导致与避免捕食相关的适应性共同进化，对于捕食者来说，克服这些防御。对抗性的共同进化关系通常不是单个捕食者和猎物之间的简单相互作用，而是多个共存物种之间复杂的相互作用网络。有毒响尾蛇和小型哺乳动物之间的共同进化导致了几种哺乳动物类群的生理毒液抗性。一般来说，蝰蛇毒液含有大量的蛇毒金属蛋白酶毒素 (SVMPs)，这些毒素会被抗性哺乳动物表达的 SVMP 抑制剂灭活。我们探索了四种共同分布物种（加利福尼亚地松鼠、布赖恩特伍德鼠、南太平洋响尾蛇、和红钻响尾蛇）从南加州的四个不同种群中收集。我们的目标是了解毒液和毒液抗性的表型和功能变化，以便将涉及两个同域捕食者 - 猎物对的系统的共同进化动力学与过去专注于单对的研究进行比较。毒液的蛋白质组学分析表明，这些响尾蛇在交配时表现出不同的表型，红钻表现出更典型的蝰蛇毒液（具有多种 SVMP），而南太平洋表现出更非典型的毒液，其中包含更广泛的非酶毒素。我们还发现，虽然两种哺乳动物的血清通常能够抑制两种响尾蛇物种的 SVMP，但抑制作用强烈依赖于蛇的种群，来自一个地理位置的蛇表达 SVMP，很少有哺乳动物对其具有抗性。此外，我们发现 Red Diamond 毒液，而不是 Woodrat 抗性，是局部适应的。我们的研究结果强调了多个捕食者和猎物之间共同进化关系的复杂性，它们在同情中表现出相似的进攻和防御策略。