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The lower reproductive tract of female mammals has several competing functions including mating, tract health maintenance, and parturition. Diverse vaginal anatomy suggests interactions between natural and sexual selection, yet despite its importance, female copulatory morphology remains under-studied. We undertook a comparative study across the species-rich mammalian order Chiroptera (bats) with a focus on the suborder Yangochiroptera (Vespertilioniformes) to examine how female vaginal features may have coevolved with male penis morphology to minimize mechanical damage to their tissues during copulation. The penis morphology is diverse, presenting great potential for post-copulatory sexual selection and coevolution with the female morphology, but vaginas have not been carefully examined. Here we test the hypotheses that vaginal thickness and collagen density have coevolved with features of the male penis, including the presence of spines and a baculum. We present histological data from females of 24 species from 7 families of bats, and corresponding data on male penis anatomy. We also examine the role of phylogenetic history in the morphological patterns we observe. We found evidence that female vaginal thickness has coevolved with the presence of penile spines, but not with baculum presence or width. Collagen density did not appear to covary with male penile features. Our findings highlight the importance of considering interactions between the sexes in influencing functional reproductive structures and examine how these structures have been under selection in bats. [ABSTRACT FROM AUTHOR]

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) and Neotoma bryanti (Bryant's woodrat) to creosote bush Larrea 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, with N. lepida persisting 20% longer than N. bryanti in 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. Read the free Plain Language Summary for this article on the Journal blog. [ABSTRACT FROM AUTHOR]

This compendium is from a symposium about reproductive biology from the female perspective, but what do we mean by the female perspective? Most obviously, since all of our speakers, and most of our contributors, are female, one meaning is that the female perspective is the view of female scientists. Our diverse contributors are from a spectrum of academic ranks (post-docs to chaired professors) and study a range of animal taxa from insects to mammals. More importantly, we want to examine reproductive biology from the perspective of female organisms themselves. What happens when we examine social behavior, physiology, or ecology strictly from the viewpoint of females? In many cases, the female-centric perspective will alter our prior interpretations. For example, with deoxyribonucleic acid fingerprinting, differences between genetic and behavioral mating-systems became obvious. The scientific community came to realize that assessing parentage is the definitive way to categorize mating systems since using male-mating strategies resulted in flawed conclusions; in fact, the female selection of which sperm is involved in conception is more important in determining parentage than mating events per se. Perhaps parentage systems rather than mating systems would be more appropriate. This difference in interpretation relative to methodology exemplifies how behavioral ecology might change if we examine systems from the female perspective; similar changes may occur for other fields. Another example comes from studies of whole-organism performance. Here, jumping, running, and swimming have been measured in males, usually with the deliberate removal of females and the major facet of female physiology, that is, reproduction. However, female biology may actually set the limits of performance given the need to carry extra weight and the extensive changes in body shape required for reproduction. Female performance is a valuable area for research. In fact, novel insights into metabolic ceilings arose from examining energetics, including metabolic rates, during lactation. In the symposium and the associated papers, our contributors explored the various ways in which a female-focused framework shifts our research conclusions and programs. As a way forward, we also include a table of sex-neutral terminology to replace terms that are currently androcentric or value-laden. [ABSTRACT FROM AUTHOR]

Philosophical truths are hidden in Lewis Carroll's nonsense poems, such as "The hunting of the snark." When the poem is used as a scientific allegory, a snark stands for the pursuit of scientific truth, while a boojum is a spurious discovery. In the study of female biology, boojums have been the result of the use of cultural stereotypes to frame hypotheses and methodologies. Although female reproduction is key for the continuation of sexually reproducing species, not only have females been understudied in many regards, but also data have commonly been interpreted in the context of now-outdated social mores. Spurious discoveries, boojums, are the result. In this article, we highlight specific gaps in our knowledge of female reproductive biology and provide a jumping-off point for future research. We discuss the promise of emerging methodologies (e.g. micro-CT scanning, high-throughput sequencing, proteomics, big-data analysis, CRISPR-Cas9, and viral vector technology) that can yield insights into previously cryptic processes and features. For example, in mice, deoxyribonucleic acid sequencing via chromatin immunoprecipitation followed by sequencing is already unveiling how epigenetics lead to sex differences in brain development. Similarly, new explorations, including microbiome research, are rapidly debunking dogmas such as the notion of the "sterile womb." Finally, we highlight how understanding female reproductive biology is well suited to the National Science Foundation's big idea, "Predicting Rules of Life." Studies of female reproductive biology will enable scholars to (1) traverse levels of biological organization from reproductive proteins at the molecular level, through anatomical details of the ovum and female reproductive tract, into physiological aspects of whole-organism performance, leading to behaviors associated with mating and maternal care, and eventually reaching population structure and ecology ; (2) discover generalizable rules such as the co-evolution of maternal-offspring phenotypes in gestation and lactation; and (3) predict the impacts of changes to reproductive timing when the reliability of environmental cues becomes unpredictable. Studies in these key areas relative to female reproduction are sure to further our understanding across a range of diverse taxa. [ABSTRACT FROM AUTHOR]

Like many scientific disciplines, the field of reproductive biology is subject to biases in terminology and research foci. For example, females are often described as coy and passive players in reproductive behaviors and are termed "promiscuous" if they engage in extra-pair copulations. Males on the other hand are viewed as actively holding territories and fighting with other males. Males are termed "multiply mating" if they mate with multiple females. Similarly, textbooks often illustrate meiosis as it occurs in males but not females. This edition of Integrative and Comparative Biology (ICB) includes a series of papers that focus on reproduction from the female perspective. These papers represent a subset of the work presented in our symposium and complementary sessions on female reproductive biology. In this round table discussion, we use a question and answer format to leverage the diverse perspectives and voices involved with the symposium in an exploration of theoretical, cultural, pedagogical, and scientific issues related to the study of female biology. We hope this dialog will provide a stepping-stone toward moving reproductive science and teaching to a more inclusive and objective framework. [ABSTRACT FROM AUTHOR]

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). In N. 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 in N. stephensi than in N. albigula (p <.01), suggesting N. stephensi produces one or more variant of CYP2B that is less efficient at processing α‐pinene. In N. stephensi, the rates of α‐pinene metabolism increased with dietary juniper and were positively correlated with CYP2B concentration. The ability of N. stephensi to elevate CYP2B concentration and rate of α‐pinene metabolism with increasing levels of juniper in the diet may facilitate juniper specialization in this species. [ABSTRACT FROM AUTHOR]

Abstract: Theory postulates that dietary specialization in mammalian herbivores is enabled by a specialized set of liver enzymes that process the high concentrations of similar plant secondary metabolites (PSMs) in the diets of specialists. To investigate whether qualitative and quantitative differences in detoxification mechanisms distinguish dietary specialists from generalists, we compared the sequence diversity and gene copy number of detoxification enzymes in two woodrat species: a generalist, the white‐throated woodrat (Neotoma albigula) and a juniper specialist, Stephens’ woodrat (N. stephensi). We focused on enzymes in the cytochrome P450 subfamily 2B (CYP2B), because previous research suggests this subfamily plays a key role in the processing of PSMs. For both woodrat species, we obtained and sequenced CYP2B cDNA, generated CYP2B phylogenies, estimated CYP2B gene copy number and created a homology model of the active site. We found that the specialist possessed on average ~5 more CYP2B gene copies than the generalist, but the specialist's CYP2B sequences were less diverse. Phylogenetic analysis of putative CYP2B homologs resolved woodrat species as reciprocally monophyletic and suggested evolutionary convergence of distinct homologs on similar key amino acid residues in both species. Homology modelling of the CYP2B enzyme suggests that interspecific differences in substrate preference and function likely result from amino acid differences in the enzyme active site. The characteristics of CYP2B in the specialist, that is greater gene copy number coupled with less sequence variation, are consistent with specialization to a narrow range of dietary toxins. [ABSTRACT FROM AUTHOR]

Allocation to reproduction is based on trade-offs between competing functions and available energy and nutrients. Because fruit is generally protein poor, strict frugivores may require additional protein during periods of investment in young and, in mammals, periods of milk production. Observations of frugivores supplementing their diets with protein-rich insects are accumulating and this is likely an underappreciated common strategy. However, it is unclear if protein augmentation is determined by seasonal abundances of high-protein food or by behavioral changes to navigate physiological demands. We present the 1st study asking if frugivorous bats supplement their diets with insects to obtain required energy and nutrients that could be used for successful reproduction. Using naturally occurring stable isotopes of nitrogen, we examine the roles of fruit versus insects to determine if these frugivorous mammals are truly specialists, we also ask how diet breadth varies with season, sex, and by reproductive state. We test 2 new hypotheses regarding when insect supplementation occurs using the well-studied largely frugivorous Jamaican fruit bat, Artibeus jamaicensis. The 1st hypothesis suggests protein augmentation occurs seasonally but independent of reproduction (H1). Alternatively, females may supplement their frugivorous diets with insects during the nitrogen-demanding periods of pregnancy and lactation (H2). Finally, we test a 3rd independent hypothesis (H3) that these bats are specialists, consistent with both H1 and H2. We found dietary shifts relative to season, reproductive state, and sex. The largest portion of insect use was by pregnant females. Surprisingly, lactating females did not consistently supplement their diets with insects and exhibited fruit-focused diets. Males exhibited the narrowest dietary breadth and nonreproductive females the greatest. Diet breath of all reproductive groups varied by month. Our data indicate that, while fruits remain an important part of the diet, insects may be an extremely valuable source of nitrogen to females during pregnancy. [ABSTRACT FROM AUTHOR]

Mammalian penises are morphologically diverse, including a highly variable and taxonomically informative baculum (os penis), and variable penile spines, both of which are possessed by many--but not all--species. To understand the evolution of genital morphologies, as well as the potential role of both the baculum, and penile spines that directly interact with female reproductive tract, we undertook a comparative study of male penile spines and their relationship with the baculum across all mammalian orders. Specifically, we investigated several factors that may explain the presence or absence of penile spines in mammals, including mating system, risk of sperm competition, female reproductive physiology, presence and width of the baculum, and phylogenetic history. We observed that the presence of both the baculum and penile spines is correlated with residual testes size, suggesting a potential role in sexual selection for these traits. We found no association between the presence of spines and mating system, or with the presence/width of the baculum, although relative testes mass was marginally associated with baculum width. We found no relationship between baculum presence or width and mating system. We also noted that spines presence or absence have an orderlevel distribution, and clear phylogenetic patterns of distribution across mammals. It is likely that spine morphology and distribution, not just presence, play an important role in genital evolution in mammals, but these features are poorly described in most groups. Quantitative data collection in most mammalian taxa would be useful to further elucidate the evolution of the complex genital morphology of this group. [ABSTRACT FROM AUTHOR]

Sperm storage, the extended maintenance of viable sperm, probably occurs in most internally fertilizing animals. Because it temporally separates mating from conception, sperm storage can be adaptive in ecologically diverse habitats and affect life histories, mating systems, cryptic female choice, sperm competition, and sexual conflict. Sperm storage can result from different selective forces acting on females and/or males, sometimes resulting in coevolution. The various criteria often used to determine the presence of sperm storage in any given taxon can result from the action of any one or all of these selective forces. Here we discuss the criteria used to study sperm storage and how we can use these to better understand the evolution of diversity in sperm-storage adaptations. [ABSTRACT FROM AUTHOR]

ABSTRACT Numerous mammalian taxa exhibit reproductive delays, pauses in reproduction that occur between mating and fertilization, between fertilization and implantation of the embryo, or after an embryo has implanted. Of the 27 mammalian orders, 9 are known to exhibit reproductive delays, including Diptrotodontia, Dasyuromorphia, Eulipotyphyta, Cingulata, Carnivora, Rodentia, Chiroptera, Lagomorpha and Cetartiodactyla. Most researchers interested in delays have focused on their evolutionary origins. However, the consequences of these delays have not been considered fully. Given the lengthening of the period over which reproduction occurs, it is possible that this unique aspect of reproduction facilitates post-copulatory sexual selection. When considered in the context of sexual selection, delays may allow sperm competition and female manipulation of fertilization (cryptic female choice) as well as other post-copulatory processes. We investigate the potential for reproductive delays to facilitate post-copulatory sexual selection and suggest avenues for research that may further our knowledge of sexual selection. We also provide a general review of reproductive delays in mammals. [ABSTRACT FROM AUTHOR]

The genomic architecture underlying the origins and maintenance of biodiversity is an increasingly accessible feature of species, due in large part to third‐generation sequencing and novel analytical toolsets. Applying these techniques to woodrats (Neotoma spp.) provides a unique opportunity to study how herbivores respond to environmental change. Neotoma bryanti and N. lepida independently achieved a major dietary feat in the aftermath of a natural climate change event: switching to the novel, toxic food source creosote bush (Larrea tridentata). To better understand the genetic mechanisms underlying this ability, we employed a trio binning sequencing approach with a N. bryanti × N. lepida F1 hybrid, allowing the simultaneous assembly of genomes representing each parental species. The resulting phased, chromosome‐level, highly complete haploid references enabled us to explore the genomic architecture of several gene families—cytochromes P450, UDP‐glucuronosyltransferases (UGTs), and ATP‐binding cassette (ABC) transporters—known to play key roles in the metabolism of naturally occurring toxic dietary compounds. In addition to duplication events in the ABCG and UGT2B subfamilies, we found expansions in three P450 gene families (2A, 2B, 3A), including the evolution of multiple novel gene islands within the 2B and 3A subfamilies, which may have provided the crucial substrate for dietary adaptation. Our assemblies demonstrate that trio binning from an F1 hybrid rodent effectively recovers parental genomes from species that diverged more than a million years ago. [ABSTRACT FROM AUTHOR]

Dipodomys microps, the chisel-toothed kangaroo rat, is heralded as one of few mammalian herbivores capable of dietary specialization. Throughout its range, the diet of D. microps is thought to consist primarily of Atriplex confertifolia (saltbush), a C4 plant, and sparing amounts of C3 plants. Using stable isotopes of carbon and nitrogen as natural diet tracers, we asked whether D. microps is an obligate specialist on saltbush. We analyzed hair samples of D. microps for isotopes from historic and recent museum specimens (N = 66). A subset of samples (N = 17) from 2017 that were associated with field notes on plant abundances were further evaluated to test how local saltbush abundance affects its inclusion in the diet of D. microps. Overall, we found that the chisel-toothed kangaroo rat facultatively specializes on saltbush and that the degree of specialization has varied over time and space. Moreover, saltbush abundance dictates its inclusion in the diet. Furthermore, roughly a quarter of the diet is comprised of insects, and over the past century, insects have become more prevalent and saltbush less prevalent in the diet. We suggest that environmental factors such as climate change and rangeland expansion have caused D. microps to include more C3 plants and insects. [ABSTRACT FROM AUTHOR]

Liver biotransformation enzymes have long been thought to enable animals to feed on diets rich in xenobiotic compounds. However, despite decades of pharmacological research in humans and rodents, little is known about hepatic gene expression in specialized mammalian herbivores feeding on toxic diets. Leveraging a recently identified population of the desert woodrat (Neotoma lepida) found to be highly tolerant to toxic creosote bush (Larrea tridentata), we explored the expression changes of suites of biotransformation genes in response to diets enriched with varying amounts of creosote resin. Analysis of hepatic RNA-seq data indicated a dose-dependent response to these compounds, including the upregulation of several genes encoding transcription factors and numerous phase I, II, and III biotransformation families. Notably, elevated expression of five biotransformation families — carboxylesterases, cytochromes P450, aldo-keto reductases, epoxide hydrolases, and UDP-glucuronosyltransferases — corresponded to species-specific duplication events in the genome, suggesting that these genes play a prominent role in N. lepida 's adaptation to creosote bush. Building on pharmaceutical studies in model rodents, we propose a hypothesis for how the differentially expressed genes are involved in the biotransformation of creosote xenobiotics. Our results provide some of the first details about how these processes likely operate in the liver of a specialized mammalian herbivore. [Display omitted] • Creosote resin induces a dose-dependent hepatic response in Neotoma lepida. • Biotransformation genes are primarily regulated by CAR, PXR, and NRF2. • Duplications are present in many upregulated biotransformation genes. • Biotransformation is accompanied by disrupted lipid and glucose metabolism. [ABSTRACT FROM AUTHOR]

Robust tick surveillance enhances diagnosis and prevention of tick-borne pathogens, yet surveillance efforts in the United States are highly uneven, resulting in large surveillance vacuums, one of which spans the state of New Mexico. As part of a larger effort to fill this vacuum, we conducted both active and passive tick sampling in New Mexico, focusing on the southern portion of the state. We conducted active tick sampling using dragging and CO₂ trapping at 45 sites across Hidalgo, Doña Ana, Otero, and Eddy counties between June 2021 to May 2022. Sampling occurred intermittently, with at least one sampling event each month from June to October 2021, pausing in winter and resuming in March through May 2022. We also conducted opportunistic, passive tick sampling in 2021 and 2022 from animals harvested by hunters or captured or collected by researchers and animals housed in animal hospitals, shelters, and farms. All pools of ticks were screened for Rickettsia rickettsii, Rickettsia parkeri, Rickettsia amblyommatis, Ehrlichia ewingii, and Ehrlichia chaffeensis. Active sampling yielded no ticks. Passive sampling yielded 497 ticks comprising Carios kelleyi from pallid bats, Rhipicephalus sanguineus from dogs, mule deer, and Rocky Mountain elk, Otobius megnini from dogs, cats, horses, and Coues deer, Dermacentor parumapertus from dogs and black-tailed jackrabbits, Dermacentor albipictus from domesticated cats, mule deer and Rocky Mountain elk, and Dermacentor spp. from American black bear, Rocky Mountain elk, and mule deer. One pool of D. parumapterus from a black-tailed jackrabbit in Luna County tested positive for R. parkeri, an agent of spotted fever rickettsiosis. Additionally, a spotted fever group Rickettsia was detected in 6 of 7 C. kelleyi pools. Two ticks showed morphological abnormalities; however, these samples did not test positive for any of the target pathogens, and the cause of the abnormalities is unknown. Passive surveillance yielded five identified species of ticks from three domestic and six wild mammal species. Our findings update tick distributions and inform the public, medical, and veterinary communities of the potential tick-borne pathogens present in southern New Mexico. [ABSTRACT FROM AUTHOR]

In sexually reproducing organisms, the genetic interests of individuals are not perfectly aligned. Conflicts among family members are prevalent since interactions involve the transfer of limited resources between interdependent players. Intrafamilial conflict has traditionally been considered along three major axes: between the sexes, between parents and offspring, and between siblings. In these interactions, conflict is expected over traits in which the resulting phenotypic value is determined by multiple family members who have only partially overlapping fitness optima. We focus on four major categories of animal reproductive mode (broadcast spawning, egg laying, live bearing, and live bearing with matrotrophy) and identify the shared phenotypes or traits over which conflict is expected, and then review the empirical literature for evidence of their occurrence. Major transitions among reproductive mode, such as a shift from external to internal fertilization, an increase in egg-retention time, modifications of embryos and mothers for nutrient transfer, the evolution of postnatal parental care, and increased interaction with the kin network, mark key shifts that both change and expand the arenas in which conflict is played out. [ABSTRACT FROM AUTHOR]

In mammals, nutrient allocation during lactation is a critical component of maternal care as milk intake promotes juvenile growth and survival, and hence maternal and offspring fitness., Milk composition varies widely across mammals and is hypothesized to have arisen via selection pressures associated with environment, diet and life history. These hypotheses have been proposed based on observations and/or cross-species comparisons that did not standardize for stage of lactation and did not consider evolutionary history of the species in analyses., We conducted the largest comparative analysis of milk composition to date accounting for phylogenetic relationships among species in order to understand the selective advantage of producing milk with specific nutritional profiles. We examined four milk constituents in association with species ecology while incorporating phylogeny in analyses., Phylogenetic signal was apparent for all milk constituents examined. After controlling for phylogeny, diet and relative lactation length explained the greatest amount of variation in milk composition. Several aspects of species' ecologies, including adaptation to arid environments, reproductive output and maternal body mass were not associated with milk composition after accounting for phylogeny., Our results suggest that milk composition is largely a function of evolutionary history, maternal nutrient intake and duration of milk production. Arriving at these conclusions was made possible by including the evolutionary relationships among species. [ABSTRACT FROM AUTHOR]

In sexually reproducing organisms, the genetic interests of individuals are not perfectly aligned. Conflicts among family members are prevalent since interactions involve the transfer of limited resources between interdependent players. Intrafamilial conflict has traditionally been considered along three major axes: between the sexes, between parents and offspring, and between siblings. In these interactions, conflict is expected over traits inwhich the resulting phenotypic value is determined by multiple family members who have only partially overlapping fitness optima. We focus on four major categories of animal reproductive mode (broadcast spawning, egg laying, live bearing, and live bearing with matrotrophy) and identify the shared phenotypes or traits over which conflict is expected, and then review the empirical literature for evidence of their occurrence. Major transitions among reproductive mode, such as a shift from external to internal fertilization, an increase in egg-retention time, modifications of embryos and mothers for nutrient transfer, the evolution of postnatal parental care, and increased interaction with the kin network, mark key shifts that both change and expand the arenas in which conflict is played out. [ABSTRACT FROM AUTHOR]

The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ~50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts. [ABSTRACT FROM AUTHOR]

Microbial detoxification of plant toxins influences the use of plants as food sources by herbivores. Stephen's woodrats (Neotoma stephensi) specialize on juniper, which is defended by oxalate, phenolics and monoterpenes, while closely related N. albigula specialize on cactus, which only contains oxalate. Woodrats maintain two gut chambers harboring dense microbial communities: a foregut chamber proximal to the major site of toxin absorption, and a cecal chamber in their hindgut. We performed several experiments to investigate the location and nature of microbial detoxification in the woodrat gut. First, we measured toxin concentrations across gut chambers of N. stephensi. Compared to food material, oxalate concentrations were immediately lower in the foregut, while concentrations of terpenes remained high in the foregut, and were lowest in the cecal chamber. We conducted metagenomic sequencing of the foregut chambers of both woodrat species and cecal chambers of N. stephensi to compare microbial functions. We found that most genes associated with detoxification were more abundant in the cecal chambers of N. stephensi. However, some genes associated with degradation of oxalate and phenolic compounds were more abundant in the foregut chambers. Thus, microbial detoxification may take place in various chambers depending on the class of chemical compound. [ABSTRACT FROM AUTHOR]