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We studied small herbivore diet composition across a sharp ecotone where two species of woodrat,Neotoma bryantiandN.lepida, come into secondary contact with one another and hybridize. We quantified woodrat dietary preference through trnLmetabarcoding of field‐collected fecal pellets and experimental choice trials. Despite gene flow, parentalN. bryantiandN. lepidamaintain distinct diets across this fine spatial scale, and across temporal scales that span both wet and dry conditions.

Neotoma bryantimaintained a more diverse diet, withFrangula californica(California coffeeberry) making up a large portion of its diet.Neotoma lepidamaintains a less diverse diet, withPrunus fasciculata(desert almond) comprising more than half of its diet. BothF. californicaandP. fasciculataare known to produce potentially toxic plant secondary compounds (PSCs), which should deter herbivory, yet these plants have relatively high nutritional value as measured by crude protein content.

Neotoma bryantiandN. lepidaconsumedF. californicaandP. fasciculata, respectively, in greater abundance than these plants are available on the landscape—indicating dietary selection. Finally, experimental preference trials revealed thatN. bryantiexhibited a preference forF. californica, whileN. lepidaexhibited a relatively stronger preference forP. fasciculata. We find thatN. bryantiexhibit a generalist herbivore strategy relative toN. lepida, which exhibit a more specialized feeding strategy in this study system.

Our results suggest that woodrats respond to fine‐scale environmental differences in plant availability that may require different metabolic strategies in order to balance nutrient acquisition while minimizing exposure to potentially toxic PSCs.

We investigated the tolerances of two species of herbivorous woodrats,Neotoma lepida(desert woodrat) andNeotoma bryanti(Bryant's woodrat) to creosote bushLarrea tridentata, a widely distributed shrub with a highly toxic resin. Woodrats were sampled from 13 locations both with and without creosote bush across a 900 km transect in the US southwest. We tested whether these woodrat populations consume creosote bush using plant metabarcoding of faeces and quantified their tolerance to creosote bush through feeding trials using chow amended with creosote resin.

Toxin tolerance was analysed in the context of population structure across collection sites with microsatellite analyses. Genetic differentiation among woodrats collected from different locations was minimal within either species. Tolerance differed substantially between the two species, withN. lepidapersisting 20% longer thanN. bryantiin feeding trials with creosote resin. Furthermore, in both species, tolerance to creosote resin was similar among woodrats near or within creosote bush habitat. In both species, woodrats collected >25 km from creosote had markedly lower tolerances to creosote resin compared to animals from within the range of creosote bush.

The results imply that mammalian herbivores are adapted to the specialized metabolites of plants in their diet, and that this tolerance can extend several kilometres outside of the range of dietary items. That is, direct ecological exposure to the specialized chemistry of particular plant species is not a prerequisite for tolerance to these compounds. These findings lay the groundwork for additional studies to investigate the genetic mechanisms underlying toxin tolerance and to identify how these mechanisms are maintained across landscape‐level scales in mammalian herbivores.