Strategies in herbivory by mammals revisited: The role of liver metabolism in a juniper specialist ( Neotoma stephensi ) and a generalist ( Neotoma albigula )

Although herbivory is widespread among mammals, few species have adopted a strategy of dietary specialization. Feeding on a single plant species often exposes herbivores to high doses of similar plant secondary metabolites (PSMs), which may exceed the animal’s detoxification capacities. Therefore, theory predicts that specialists will have unique detoxification mechanisms to process high levels of dietary toxins. To evaluate this hypothesis, we compared liver metabolism of a juniper specialist, Neotoma stephensi (diet >85% juniper), to that of a sympatric generalist, N. albigula (diet ≤30% juniper). Specifically, we quantified the content of a key detoxification enzyme, cytochrome P450 2B (CYP2B) in liver microsomes, as well as the microsomal turnover of α-pinene, the most abundant terpene in the juniper species consumed by the specialist woodrat. In both Neotoma species, a 30% juniper diet increased CYP2B content (2-3x) and α-pinene turnover rates (4-fold). In N. stephensi, higher levels of dietary juniper (60% and 100%) further induced CYP2B content and increased turnover rates of α-pinene. Although no species-specific differences in α-pinene turnover rates were observed at 30% dietary juniper, CYP2B content was 1.7x higher in N. stephensi than in N. albigula (p<0.01). In N. stephensi, the rates of α-pinene turnover increased with dietary juniper and were positively correlated with CYP2B content. The ability of N. stephensi to elevate CYP2B content and rate of α-pinene turnover with increasing levels of juniper in the diet (from 30-100%) may facilitate juniper specialization in this species.

尽管植食性在哺乳动物中广泛存在，但极少有物种演化出食性特化的取食策略。仅取食单一植物物种的植食动物常会暴露于高剂量的同类植物次生代谢物（plant secondary metabolites, PSMs）中，其浓度可能超出动物自身的解毒能力。因此，相关理论预测，食性特化类群应具备独特的解毒机制，以处理高水平的膳食毒素。为验证这一假说，我们对比了专食杜松的斯蒂芬林鼠（Neotoma stephensi，膳食组成中杜松占比超85%）与同域分布的广食性物种白喉林鼠（Neotoma albigula，膳食中杜松占比≤30%）的肝脏代谢特征。具体而言，我们定量测定了肝微粒体中关键解毒酶细胞色素P450 2B（cytochrome P450 2B, CYP2B）的含量，以及α-蒎烯的微粒体代谢速率——α-蒎烯是该专食性林鼠所取食的杜松物种中含量最丰富的萜类物质。在两种林鼠属物种中，饲喂30%杜松的日粮均可使CYP2B含量提升2~3倍，同时使α-蒎烯的代谢速率提升4倍。在斯蒂芬林鼠中，更高比例的杜松日粮（60%和100%）可进一步诱导CYP2B含量上调，并提升α-蒎烯的代谢速率。尽管在饲喂30%杜松日粮时，两种物种的α-蒎烯代谢速率未出现物种特异性差异，但斯蒂芬林鼠的CYP2B含量较白喉林鼠高出1.7倍（p<0.01）。在斯蒂芬林鼠体内，α-蒎烯的代谢速率随日粮中杜松占比升高而提升，且与CYP2B含量呈显著正相关。斯蒂芬林鼠可随日粮杜松占比（30%至100%）提升而上调CYP2B含量与α-蒎烯代谢速率，这一能力或助力该物种演化出杜松专食的食性策略。