Title: Differences in dietary composition and preference maintained despite gene flow across a woodrat hybrid zone
Abstract
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,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.
Dearing, M. Denise; Orr, Teri J.; Klure, Dylan M.; Greenhalgh, Robert; Weinstein, Sara B.; Stapleton, Tess E.; Yamada, KayLene Y. H.; Nelson, Madeleine D.; Doolin, Margaret L.; Nielsen, Danny P.; et al(
, Functional Ecology)
Abstract
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,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.
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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 (genusNeotoma).Neotoma stephensiis an obligate specialist on one‐seeded juniper (Juniperus monosperma).Neotoma lepidais 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. stephensiexcreted a unique pattern of Phase I metabolites when fed its native juniper, whileN. lepidaexcreted 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. stephensiutilized less glucuronidation thanN. lepidawhen 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.
Jesmer, Brett R.; Kauffman, Matthew J.; Murphy, Melanie A.; Goheen, Jacob R.; Jackson, ed., Andrew(
, Journal of Animal Ecology)
Abstract
Despite the shared prediction that the width of a population's dietary niche expands as food becomes limiting, the Niche Variation Hypothesis (NVH) and Optimal Foraging Theory (OFT) offer contrasting views about how individuals alter diet selection when food is limited.
Classical OFT predicts that dietary preferences do not change as food becomes limiting, so individuals expand their diets as they compensate for a lack of preferred foods. In contrast, the NVH predicts that among‐individual variation in cognition, physiology or morphology create functional trade‐offs in foraging efficiency, thereby causing individuals to specialize on different subsets of food as food becomes limiting.
To evaluate (a) the predictions of the NVH and OFT and (b) evidence for physiological and cognitive‐based functional trade‐offs, we used DNA microsatellites and metabarcoding to quantify the diet, microbiome and genetic relatedness (a proxy for social learning) of 218 mooseAlces alcesacross six populations that varied in their degree of food limitation.
Consistent with both the NVH and OFT, dietary niche breadth increased with food limitation. Increased diet breadth of individuals—rather than increased diet specialization—was strongly correlated with both food limitation and dietary niche breadth of populations, indicating that moose foraged in accordance with OFT. Diets were not constrained by inheritance of the microbiome or inheritance of diet selection, offering support for the little‐tested hypothesis that functional trade‐offs in food use (or lack thereof) determine whether populations adhere to the predictions of the NVH or OFT.
Our results indicate that both the absence of strong functional trade‐offs and the digestive physiology of ruminants provide contexts under which populations should forage in accordance with OFT rather than the NVH. Also, because dietary niche width increased with increased food limitation, OFT and the NVH provide theoretical support for the notion that plant–herbivore interaction networks are plastic rather than static, which has important implications for understanding interspecific niche partitioning. Lastly, because population‐level dietary niche breadth and calf recruitment are correlated, and because calf recruitment can be a proxy for food limitation, our work demonstrates how diet data can be employed to understand a populations' proximity to carrying capacity.
Pansu, Johan; Guyton, Jennifer A.; Potter, Arjun B.; Atkins, Justine L.; Daskin, Joshua H.; Wursten, Bart; Kartzinel, Tyler R.; Pringle, Robert M.; Chapman, ed., Samantha(
, Journal of Ecology)
Abstract
Megafauna assemblages have declined or disappeared throughout much of the world, and many efforts are underway to restore them. Understanding the trophic ecology of such reassembling systems is necessary for predicting recovery dynamics, guiding management, and testing general theory. Yet, there are few studies of recovering large‐mammal communities, and fewer still that have characterized food‐web structure with high taxonomic resolution.
In Gorongosa National Park, large herbivores have rebounded from near‐extirpation following the Mozambican Civil War (1977–1992). However, contemporary community structure differs radically from the prewar baseline: medium‐sized ungulates now outnumber larger bodied species, and several apex carnivores remain locally extinct.
We used DNA metabarcoding to quantify diet composition of Gorongosa’s 14 most abundant large‐mammal populations. We tested five hypotheses: (i) the most abundant populations exhibit greatest individual‐level dietary variability; (ii) these populations also have the greatest total niche width (dietary diversity); (iii) interspecific niche overlap is high, with the diets of less‐abundant species nested within those of more‐abundant species; (iv) partitioning of forage species is stronger in more structurally heterogeneous habitats; and (v) selectivity for plant taxa converges within guilds and digestive types, but diverges across them.
Abundant (and narrow‐mouthed) populations exhibited higher among‐individual dietary variation, but not necessarily the greatest dietary diversity. Interspecific dietary overlap was high, especially among grazers and in structurally homogenous habitat, whereas niche separation was more pronounced among browsers and in heterogeneous habitat. Patterns of selectivity were similar for ruminants—grazers and browsers alike—but differed between ruminants and non‐ruminants.
Synthesis. The structure of this recovering food web was consistent with several hypotheses predicated on competition, habitat complexity, and herbivore traits, but it differed from patterns observed in more intact assemblages. We propose that intraspecific competition in the fastest‐recovering populations has promoted individual variation and a more nested food web, wherein rare species use subsets of foods eaten by abundant species, and that this scenario is reinforced by weak predation pressure. Future work should test these conjectures and analyse how the taxonomic dietary niche axis studied here interacts with other mechanisms of diet partitioning to affect community reassembly following wildlife declines.
Orr, Teri J.; Kitanovic, Smiljka; Schramm, Katharina M.; Skopec, Michele M.; Wilderman, P. Ross; Halpert, James R.; Dearing, M. Denise(
, Molecular Ecology)
Abstract
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 plant secondary metabolites (PSMs), which may exceed the animal's detoxification capacities. Theory predicts that specialists will have unique detoxification mechanisms to process high levels of dietary toxins. To evaluate this hypothesis, we compared liver microsomal metabolism of a juniper specialist,Neotoma stephensi(diet >85% juniper), to a generalist,N. albigula(diet ≤30% juniper). Specifically, we quantified the concentration of a key detoxification enzyme, cytochrome P450 2B (CYP2B) in liver microsomes, and the metabolism of α‐pinene, the most abundant terpene in the juniper species consumed by the specialist woodrat. In both species, a 30% juniper diet increased the total CYP2B concentration (2–3×) in microsomes and microsomal α‐pinene metabolism rates (4‐fold). InN. stephensi, higher levels of dietary juniper (60% and 100%) further induced CYP2B and increased metabolism rates of α‐pinene. Although no species‐specific differences in metabolism rates were observed at 30% dietary juniper, total microsomal CYP2B concentration was 1.7× higher inN. stephensithan inN. albigula(p < .01), suggestingN. stephensiproduces one or more variant of CYP2B that is less efficient at processing α‐pinene. InN. stephensi, the rates of α‐pinene metabolism increased with dietary juniper and were positively correlated with CYP2B concentration. The ability ofN. stephensito elevate CYP2B concentration and rate of α‐pinene metabolism with increasing levels of juniper in the diet may facilitate juniper specialization in this species.
Nielsen, Danny P., and Matocq, Marjorie D. Differences in dietary composition and preference maintained despite gene flow across a woodrat hybrid zone. Ecology and Evolution 11.9 Web. doi:10.1002/ece3.7399.
Nielsen, Danny P., & Matocq, Marjorie D. Differences in dietary composition and preference maintained despite gene flow across a woodrat hybrid zone. Ecology and Evolution, 11 (9). https://doi.org/10.1002/ece3.7399
Nielsen, Danny P., and Matocq, Marjorie D.
"Differences in dietary composition and preference maintained despite gene flow across a woodrat hybrid zone". Ecology and Evolution 11 (9). Country unknown/Code not available: Wiley Blackwell (John Wiley & Sons). https://doi.org/10.1002/ece3.7399.https://par.nsf.gov/biblio/10452925.
@article{osti_10452925,
place = {Country unknown/Code not available},
title = {Differences in dietary composition and preference maintained despite gene flow across a woodrat hybrid zone},
url = {https://par.nsf.gov/biblio/10452925},
DOI = {10.1002/ece3.7399},
abstractNote = {Abstract 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,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.},
journal = {Ecology and Evolution},
volume = {11},
number = {9},
publisher = {Wiley Blackwell (John Wiley & Sons)},
author = {Nielsen, Danny P. and Matocq, Marjorie D.},
}
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