Ecotones, characterized by adjacent yet distinct biotic communities, provide natural laboratories in which to investigate how environmental selection influences the ecology and evolution of organisms. For wild herbivores, differential plant availability across sharp ecotones may be an important source of dietary‐based selection. We studied small herbivore diet composition across a sharp ecotone where two species of woodrat, 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.
Little is known about the tolerances of mammalian herbivores to plant specialized metabolites across landscapes. We investigated the tolerances of two species of herbivorous woodrats, 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, with 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.
Read the free
- Award ID(s):
- 1656497
- NSF-PAR ID:
- 10380740
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Functional Ecology
- Volume:
- 36
- Issue:
- 8
- ISSN:
- 0269-8463
- Page Range / eLocation ID:
- p. 2119-2131
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Neotoma bryanti andN .lepida , come into secondary contact with one another and hybridize. We quantified woodrat dietary preference through trnL metabarcoding of field‐collected fecal pellets and experimental choice trials. Despite gene flow, parentalN. bryanti andN. lepida maintain distinct diets across this fine spatial scale, and across temporal scales that span both wet and dry conditions.Neotoma bryanti maintained a more diverse diet, withFrangula californica (California coffeeberry) making up a large portion of its diet.Neotoma lepida maintains a less diverse diet, withPrunus fasciculata (desert almond) comprising more than half of its diet. BothF. californica andP. fasciculata are 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 bryanti andN. lepida consumedF. californica andP. fasciculata , respectively, in greater abundance than these plants are available on the landscape—indicating dietary selection. Finally, experimental preference trials revealed thatN. bryanti exhibited a preference forF. californica , whileN. lepida exhibited a relatively stronger preference forP. fasciculata . We find thatN. bryanti exhibit a generalist herbivore strategy relative toN. lepida , which exhibit a more specialized feeding strategy in this study system. -
more » « less
Abstract Herbivory is common in mammals, yet our understanding of detoxification processes used by mammals to biotransform plant secondary compounds (PSCs) is limited. Specialist herbivores are thought to have evolved detoxification mechanisms that rely more heavily on energetically cheap Phase I biotransformation reactions to process high levels of PSCs in their diets. We explored this hypothesis by comparing the urinary metabolite patterns of two specialist herbivores (genus
Neotoma) .Neotoma stephensi is an obligate specialist on one‐seeded juniper (Juniperus monosperma ).Neotoma lepida is a generalist forager across its range, yet populations in the Great Basin specialize on Utah juniper (J. osteosperma ). While both juniper species have high levels of terpenes, the terpene profiles and quantities differ between the two. Individuals from both woodrat species were fed diets of each juniper in a cross‐over design. Urine, collected over a 24‐h period, was extracted and analyzed in an untargeted metabolomics approach using both GC‐MS and HPLC‐MS/MS. The obligate specialistN. stephensi excreted a unique pattern of Phase I metabolites when fed its native juniper, whileN. lepida excreted a unique pattern of Phase II metabolites when fed its native juniper. Both woodrat species utilized the Phase II metabolic pathway of glucuronidation more heavily when consuming the more chemically diverseJ. osteosperma , andN. stephensi utilized less glucuronidation thanN. lepida when consumingJ. monosperma . These results are consistent with the hypothesis that obligate specialists may have evolved unique and efficient biotransformation mechanisms for dealing with PSCs in their diet. -
more » « less
Abstract Hybridization is a common process that has broadly impacted the evolution of multicellular eukaryotes; however, how ecological factors influence this process remains poorly understood. Here, we report the findings of a 3-year recapture study of the Bryant’s woodrat (Neotoma bryanti) and desert woodrat (Neotoma lepida), two species that hybridize within a creosote bush (Larrea tridentata) shrubland in Whitewater, CA, USA. We used a genotype-by-sequencing approach to characterize the ancestry distribution of individuals across this hybrid zone coupled with Cormack–Jolly–Seber modeling to describe demography. We identified a high frequency of hybridization at this site with ~40% of individuals possessing admixed ancestry, which is the result of multigenerational backcrossing and advanced hybrid-hybrid crossing. F1, F2, and advanced generation hybrids had apparent survival rates similar to parental N. bryanti, while parental and backcross N. lepida had lower apparent survival rates and were far less abundant. Compared to bimodal hybrid zones where hybrids are often rare and selected against, we find that hybrids at Whitewater are common and have comparable survival to the dominant parental species, N. bryanti. The frequency of hybridization at Whitewater is therefore likely limited by the abundance of the less common parental species, N. lepida, rather than selection against hybrids.
-
more » « less
Abstract Large and small mammalian herbivores are present in most vegetated areas in the Arctic and often have large impacts on plant community composition and ecosystem functioning. The relative importance of different herbivores and especially how their specific impact on the vegetation varies across the Arctic is however poorly understood.
Here, we investigate how large and small herbivores influence vegetation density and plant community composition in four arctic vegetation types in Scandinavia and Alaska. We used a unique set of exclosures, excluding only large (reindeer and muskoxen) or all mammalian herbivores (also voles and lemmings) for at least 20 years.
We found that mammalian herbivores in general decreased leaf area index, NDVI, and abundance of vascular plants in all four locations, even though the strength of the effect and which herbivore type caused these effects differed across locations. In three locations, herbivore presence caused contrasting plant communities, but not in the location with lowest productivity. Large herbivores had a negative effect on plant height, whereas small mammalian herbivores increased species diversity by decreasing dominance of the initially dominating plant species. Above‐ or belowground disturbances caused by herbivores were found to play an important role in shaping the vegetation in all locations.
Synthesis: Based on these results, we conclude that both small and large mammalian herbivores influence vegetation in Scandinavia and Alaska in a similar way, some of which can mitigate effects of climate change. We also see important differences across locations, but these depend rather on local herbivore and plant community composition than large biogeographical differences among continents. -
more » « less
Abstract Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L‐tyrosine and its role as a defence against herbivores.
We examined overexpression of tyrosine in 97 species of
Inga (Fabaceae), a genus of tropical trees, at five sites throughout the Neotropics. We predicted that tyrosine could act as an anti‐herbivore defence because concentrations of 4% tyrosine in artificial diets halved larval growth rates. We also collected insect herbivores to determine if tyrosine and its derivatives influenced host associations.Overexpression of tyrosine was only present in a single lineage comprising 21 species, with concentrations ranging from 5% to 20% of the leaf dry weight. Overexpression was pronounced in expanding but not in mature leaves. Despite laboratory studies showing toxicity of L‐tyrosine,
Inga species with tyrosine suffered higher levels of herbivory. We therefore hypothesize that overexpression is only favoured in species with less effective secondary metabolites. Some tyrosine‐producing species also contained secondary metabolites that are derived from tyrosine: tyrosine‐gallates, tyramine‐gallates and DOPA‐gallates. Elevated levels of transcripts of prephenate dehydrogenase, an enzyme in the tyrosine biosynthetic pathway that is insensitive to negative feedback from tyrosine, were found only in species that overexpress tyrosine or related gallates. Different lineages of herbivores showed contrasting responses to the overexpression of tyrosine and its derived secondary metabolites in their host plants.Synthesis . We propose that overexpression of some primary metabolites can serve as a chemical defence against herbivores, and are most likely to be selected for in species suffering high herbivory due to less effective secondary metabolites. Overexpression may be the first evolutionary step in the transition to the production of more derived secondary metabolites. Presumably, derived compounds would be more effective and less costly than free tyrosine as anti‐herbivore defences.
