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  1. Abstract

    We report preliminary evidence of a symbiotic parabasalian protist in the guts of Peruvian mimic poison frog (Ranitomeya imitator) tadpoles. This species has biparental care and egg-feeding of tadpoles, while the relatedR. variabilisconsumes the ancestral detritus diet in their nursery pools. Each species’ diet was experimentally switched, in the field and lab. Analyses of gut gene expression revealed elevated expression of proteases in theR. imitatorfield egg-fed treatment. These digestive proteins came from parabasalians, a group of protists known to form symbiotic relationships with hosts that enhance digestion. Genes that code for these digestive proteins are not present in theR. imitatorgenome, and phylogenetic analyses indicate that these mRNA sequences are from parabasalians. Bar-coding analyses of the tadpole microbiomes further confirmed this discovery. Our findings indicate the presence of parabasalian symbiotes in the intestines of theR. imitatortadpoles, that may aid the tadpoles in protein/lipid digestion in the context of an egg diet. This may have enabled the exploitation of a key ecological niche, allowingR. imitatorto expand into an area with ecologically similar species (e.g.,R. variabilisandR. summersi). In turn, this may have enabled a Müllerian mimetic radiation, one of only a few examples of this phenomenon in vertebrates.

     
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  2. Abstract

    Researchers have long debated which estimator of relatedness best captures the degree of relationship between two individuals. In the genomics era, this debate continues, with relatedness estimates being sensitive to the methods used to generate markers, marker quality, and levels of diversity in sampled individuals. Here, we compare six commonly used genome‐based relatedness estimators (kinship genetic distance [KGD], Wang maximum likelihood [TrioML], Queller and Goodnight [Rxy], Kinship INference for Genome‐wide association studies [KING‐robust), and pairwise relatedness [RAB], allele‐sharing coancestry [AS]) across five species bred in captivity–including three birds and two mammals–with varying degrees of reliable pedigree data, using reduced‐representation and whole genome resequencing data. Genome‐based relatedness estimates varied widely across estimators, sequencing methods, and species, yet the most consistent results for known first order relationships were found usingRxy,RAB, and AS. However, AS was found to be less consistently correlated with known pedigree relatedness than eitherRxyorRAB. Our combined results indicate there is not a single genome‐based estimator that is ideal across different species and data types. To determine the most appropriate genome‐based relatedness estimator for each new data set, we recommend assessing the relative: (1) correlation of candidate estimators with known relationships in the pedigree and (2) precision of candidate estimators with known first‐order relationships. These recommendations are broadly applicable to conservation breeding programmes, particularly where genome‐based estimates of relatedness can complement and complete poorly pedigreed populations. Given a growing interest in the application of wild pedigrees, our results are also applicable to in situ wildlife management.

     
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  3. Abstract

    How intensely animals use habitat features depends on their functional properties (i.e., how the feature influences fitness) and the spatial and temporal scale considered. For herbivores, habitat use is expected to reflect the competing risks of starvation, predation, and thermal stress, but the relative influence of each functional property is expected to vary in space and time. We examined how a dietary and habitat specialist, the pygmy rabbit (Brachylagus idahoensis), used these functional properties of its sagebrush habitat—food quality, security, and thermal refuge—at two hierarchical spatial scales (microsite and patch) across two seasons (winter and summer). At the microsite and patch scales, we determined which plant functional traits predicted the number of bites (i.e., foraging) by pygmy rabbits and the number of their fecal pellets (i.e., general habitat use). Pygmy rabbits used microsites and patches more intensely that had higher crude protein and aerial concealment cover and were closer to burrows. Food quality was more influential when rabbits used microsites within patches. Security was more influential in winter than summer, and more at Cedar Gulch than Camas. However, the influence of functional properties depended on phytochemical and structural properties of sagebrush and was not spatiotemporally consistent. These results show function‐dependent habitat use that varied according to specific activities by a central‐place browsing herbivore. Making spatially explicit predictions of the relative value of habitat features that influence different types of habitat use (i.e., foraging, hiding, and thermoregulating) will improve how we predict patterns of habitat use by herbivores and how we monitor and manage functional traits within habitats for wildlife.

     
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  4. Abstract

    Congeneric species often share ecological niche space resulting in competitive interactions that either limit co-occurrence or lead to niche partitioning. Differences in fundamental nutritional niches mediated through character displacement or isolation during evolution are potential mechanisms that could explain overlapping distribution patterns of congenerics. We directly compared nutritional requirements and tolerances that influence the fundamental niche of mule (Odocoileus hemionus) and white-tailed deer (O. virginianus), which occur in allopatry and sympatry in similar realized ecological niches across their ranges in North America. Digestible energy and protein requirements and tolerances for plant fiber and plant secondary metabolites (PSMs) of both deer species were quantified using in vivo digestion and intake tolerance trials with six diets ranging in content of fiber, protein, and PSMs using tractable deer raised under identical conditions in captivity. We found that compared with white-tailed deer, mule deer required 54% less digestible protein and 21% less digestible energy intake per day to maintain body mass and nitrogen balance. In addition, they had higher fiber, energy, and dry matter digestibility and produced glucuronic acid (a byproduct of PSM detoxification) at a slower rate when consuming the monoterpene α-pinene. The mule deers’ enhanced physiological abilities to cope with low-quality, chemically defended forages relative to white-tailed deer might minimize potential competitive interactions in shared landscapes and provide a modest advantage to mule deer in habitats dominated by low-quality forages.

     
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  5. Abstract

    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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  6. Abstract

    Local adaptation can occur when spatially separated populations are subjected to contrasting environmental conditions. Historically, understanding the genetic basis of adaptation has been difficult, but increased availability of genome‐wide markers facilitates studies of local adaptation in non‐model organisms of conservation concern. The pygmy rabbit (Brachylagus idahoensis) is an imperiled lagomorph that relies on sagebrush for forage and cover. This reliance has led to widespread population declines following reductions in the distribution of sagebrush, leading to geographic separation between populations. In this study, we used >20,000 single nucleotide polymorphisms, genotype‐environment association methods, and demographic modeling to examine neutral genetic variation and local adaptation in the pygmy rabbit in Nevada and California. We identified 308 loci as outliers, many of which had functional annotations related to metabolism of plant secondary compounds. Likewise, patterns of spatial variation in outlier loci were correlated with landscape and climatic variables including proximity to streams, sagebrush cover, and precipitation. We found that populations in the Mono Basin of California probably diverged from other Great Basin populations during late Pleistocene climate oscillations, and that this region is adaptively differentiated from other regions in the southern Great Basin despite limited gene flow and low effective population size. Our results demonstrate that peripherally isolated populations can maintain adaptive divergence.

     
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  7. Abstract

    An increasing number of ecological studies have used chemical diversity as a functionally relevant, scalable measure of phytochemical mixtures, demanding more rigorous attention to how chemical diversity is estimated. Most studies have focused on the composition of phytochemical mixtures and have largely ignored structural concerns, which may have greater importance for ecological function. Here, we explore the development of structural complexity and compositional diversity resulting from different biotic and abiotic interactions inPiper kelleyiTepe (Piperaceae). We also describe how variation in structural complexity and compositional diversity differs between two congeners,P. kelleyiandP.reticulatum. To better interpret these results, we have developed a framework for interpreting these dimensions of chemical diversity in phytochemical mixtures.

    We used the tropical shrub,P.kelleyi, as a model system to examine interactions between ecological factors and dimensions of phytochemical diversity. We also compared compositional diversity and metabolic complexity inP. kelleyiandP. reticulatumusing liquid chromatography and1H NMR, respectively, to examine trade‐offs between compositional diversity and structural complexity. A framework is provided to generate meaningful estimates of the structural complexity of phytochemical mixtures as measured by1H NMR.

    Piperis an abundant plant genus that supports diverse insect communities throughout the tropics. Subtle changes in understorey forest light were associated with increases in herbivory that directly increased compositional diversity and indirectly decreased structural complexity inP. kelleyi. This was attributed to the production of oxidation products resulting from herbivory‐driven decomposition of structurally complex defence compounds. This type of complex result would remain undetected using standard chemical ecology approaches and accounts for the detailed molecular changes that are likely to affect species interactions.

    Synthesis. Our quantitative framework provides a method for considering trade‐offs between structural complexity and compositional diversity and the interpretation of analytical approaches for each. This methodology will provide new theoretical insights and a more sophisticated model for examining the ecology and evolution of chemically mediated interactions.

     
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  8. 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.

     
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  9. Abstract

    Telomere length dynamics are an established biomarker of health and ageing in animals. The study of telomeres in numerous species has been facilitated by methods to measure telomere length by real‐time quantitative PCR (qPCR). In this method, telomere length is determined by quantifying the amount of telomeric DNA repeats in a sample and normalizing this to the total amount of genomic DNA. This normalization requires the development of genomic reference primers suitable for qPCR, which remains challenging in nonmodel organism with genomes that have not been sequenced. Here we report reference primers that can be used in qPCR to measure telomere lengths in any vertebrate species. We designed primer pairs to amplify genetic elements that are highly conserved between evolutionarily distant taxa and tested them in species that span the vertebrate tree of life. We report five primer pairs that meet the specificity and reproducibility standards of qPCR. In addition, we demonstrate an approach to choose the best primers for a given species by testing the primers on multiple individuals within a species and then applying an established computational tool. These reference primers can facilitate qPCR‐based telomere length measurements in any vertebrate species of ecological or economic interest.

     
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  10. Free, publicly-accessible full text available April 1, 2024