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1. Metabolomic evidence of independent biotransformation pathways for terpenes in two specialist mammalian herbivores (genus Neotoma )

   https://doi.org/10.1111/1749-4877.12734  

   SCHRAMM, Katharina ; SKOPEC, Michele ; DEARING, Denise ( June 2023 , Integrative Zoology)

   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.

    

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2. Multigenerational backcrossing and introgression between two woodrat species at an abrupt ecological transition

   https://doi.org/10.1111/mec.16056  

   Jahner, Joshua P. ; Parchman, Thomas L. ; Matocq, Marjorie D. ( July 2021 , Molecular Ecology)

   When organisms experience secondary contact after allopatric divergence, genomic regions can introgress differentially depending on their relationships with adaptation, reproductive isolation, recombination, and drift. Analyses of genome‐wide patterns of divergence and introgression could provide insight into the outcomes of hybridization and the potential relationship between allopatric divergence and reproductive isolation. Here, we generate population genetic data (26,262 SNPs; 353 individuals) using a reduced‐representation sequencing approach to quantify patterns of ancestry, differentiation, and introgression between a pair of ecologically distinct mammals—the desert woodrat (N.lepida) and Bryant's woodrat (N.bryanti)—that hybridize at a sharp ecotone in southern California. Individual ancestry estimates confirmed that hybrids were rare in this bimodal hybrid zone, and entirely consisted of a few F₁individuals and a broad range of multigenerational backcrosses. Genomic cline analyses indicated more than half of loci had elevated introgression from one genomic background into the other. However, introgression was not associated with relative or absolute measures of divergence, and loci with extreme values for both were not typically found near detoxification enzymes previously implicated in dietary specialization for woodrats. The decoupling of differentiation and introgression suggests that processes other than adaptation, such as drift, may underlie the extreme clines at this contact zone.

    

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3. Variable hybridization outcomes in trout are predicted by historical fish stocking and environmental context

   https://doi.org/10.1111/mec.15175  

   Mandeville, Elizabeth G. ; Walters, Annika W. ; Nordberg, Brittany J. ; Higgins, Karly H. ; Burckhardt, Jason C. ; Wagner, Catherine E. ( August 2019 , Molecular Ecology)

   Hybridization can profoundly affect the genomic composition and phenotypes of closely related species, and provides an opportunity to identify mechanisms that maintain reproductive isolation between species. Recent evidence suggests that hybridization outcomes within a species pair can vary across locations. However, we still do not know how variable outcomes of hybridization are across geographic replicates, and what mechanisms drive that variation. In this study, we described hybridization outcomes across 27 locations in the North Fork Shoshone River basin (Wyoming, USA) where native Yellowstone cutthroat trout and introduced rainbow trout co‐occur. We used genomic data and hierarchical Bayesian models to precisely identify ancestry of hybrid individuals. Hybridization outcomes varied across locations. In some locations, only rainbow trout and advanced backcrossed hybrids towards rainbow trout were present, while trout in other locations had a broader range of ancestry, including both parental species and first‐generation hybrids. Later‐generation intermediate hybrids were rare relative to backcrossed hybrids and rainbow trout individuals. Using an individual‐based simulation, we found that outcomes of hybridization in the North Fork Shoshone River basin deviate substantially from what we would expect under null expectations of random mating and no selection against hybrids. Since this deviation implies that some mechanisms of reproductive isolation function to maintain parental taxa and a diversity of hybrid types, we then modelled hybridization outcomes as a function of environmental variables and stocking history that are likely to affect prezygotic barriers to hybridization. Variables associated with history of fish stocking were the strongest predictors of hybridization outcomes, followed by environmental variables that might affect overlap in spawning time and location.

    

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4. Differences in dietary composition and preference maintained despite gene flow across a woodrat hybrid zone

   https://doi.org/10.1002/ece3.7399  

   Nielsen, Danny P. ; Matocq, Marjorie D. ( March 2021 , Ecology and Evolution)

   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.

    

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5. Hybrid enrichment of adaptive variation revealed by genotype–environment associations in montane sedges

   https://doi.org/10.1111/mec.16502  

   Hodel, Richard G. J. ; Massatti, Rob ; Knowles, L. Lacey ( June 2022 , Molecular Ecology)

   The role of hybridization in diversification is complex and may result in many possible outcomes. Not only can hybridization produce new lineages, but those lineages may contain unique combinations of adaptive genetic variation derived from parental taxa that allow hybrid‐origin lineages to occupy unique environmental space relative to one (or both) parent(s). We document such a case of hybridization between two sedge species,Carex novaandCarex nelsonii(Cyperaceae), that occupy partially overlapping environmental space in the southern Rocky Mountains, USA. In the region hypothesized to be the origin of the hybrid lineage, one parental taxon (C. nelsonii) is at the edge of its environmental tolerance. Hybrid‐origin individuals display mixed ancestry between the parental taxa—of nearly 7000 unlinked loci sampled, almost 30% showed evidence of excess ancestry from one parental lineage—approximately half displayed a genomic background skewed towards one parent, and half skewed towards the other. To test whether excess ancestry loci may have conferred an adaptive advantage to the hybrid‐origin lineage, we conducted genotype–environment association analyses on different combinations of loci—with and without excess ancestry—and with multiple contrasts between the hybrids and parental taxa. Loci with skewed ancestry showed significant environmental associations distinguishing the hybrid lineage from one parent (C. nelsonii), whereas loci with relatively equal representation of parental ancestries showed no such environmental associations. Moreover, the overwhelming majority of candidate adaptive loci with respect to environmental gradients also had excess ancestry from a parental lineage, implying these loci have facilitated the persistence of the hybrid lineage in an environment unsuitable to at least one parent.

    

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