Asymmetric mate preference and reproductive interference mediate climate-induced changes in mate availability in a small mammal hybrid zone.

Range expansion and contraction are among the most common biotic responses to changing environmental conditions, yet much is to be learned about the mechanisms that underlie range-edge population dynamics, especially when those areas are points of secondary contact between closely related species. Here, we present field-measured parentage data that document the reproductive outcomes of changes in mate availability at a secondary contact zone between two species of woodrat in the genus Neotoma. Changes in mate availability resulted from drought-driven differential survival between the species and their hybrids. As the availability of conspecific mates declined, rates of hybridization increased, leading to the accumulation of admixed individuals in the zone of contact. Patterns of reproductive success in the wild appear to be the result of a combination of both pre-mating isolation and post-zygotic selection resulting from genomic incompatibilities between the parental lineages. Evidence of asymmetric mate preference between the parental lineages came from both skewed reproductive output in the field and laboratory preference trials. Moreover, partial genomic incompatibility was evident from the near-zero reproductive success of F1 males and because nearly all surviving hybrids had one pure parent. Nonetheless, high reproductive success of F1 females and backcrossing in both parental directions allow for introgression between the parental species. These findings reveal how climate change may alter evolutionary outcomes for species at the edge of their ranges through an interplay of behavioral, demographic, and genetic mechanisms.

New uses for ancient middens: bridging ecological and evolutionary perspectives.

Rodent middens provide a fine-scale spatiotemporal record of plant and animal communities over the late Quaternary. In the Americas, middens have offered insight into biotic responses to past environmental changes and historical factors influencing the distribution and diversity of species. However, few studies have used middens to investigate genetic or ecosystem level responses. Integrating midden studies with neoecology and experimental evolution can help address these gaps and test mechanisms underlying eco-evolutionary patterns across biological and spatiotemporal scales. Fully realizing the potential of middens to answer cross-cutting ecological and evolutionary questions and inform conservation goals in the Anthropocene will require a collaborative research community to exploit existing midden archives and mount new campaigns to leverage midden records globally.

Hybridization in the absence of an ecotone favors hybrid success in woodrats (Neotoma spp.).

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.

The gut microbiome reflects ancestry despite dietary shifts across a hybrid zone.

The microbiome is critical to an organism's phenotype, and its composition is shaped by, and a driver of, eco-evolutionary interactions. We investigated how host ancestry, habitat and diet shape gut microbial composition in a mammalian hybrid zone between Neotoma lepida and N. bryanti that occurs across an ecotone between distinct vegetation communities. We found that habitat is the primary determinant of diet, while host genotype is the primary determinant of the gut microbiome-a finding further supported by intermediate microbiome composition in first-generation hybrids. Despite these distinct primary drivers, microbial richness was correlated with diet richness, and individuals that maintained higher dietary richness had greater gut microbial community stability. Both relationships were stronger in the relative dietary generalist of the two parental species. Our findings show that host ancestry interacts with dietary habits to shape the microbiome, ultimately resulting in the phenotypic plasticity that host-microbial interactions allow.

Reevaluation of the phylogenetic relationships among Neotomini rodents (Hodomys, Neotoma, and Xenomys) and comments on the woodrat classification.

The woodrats or packrats of the genus Neotoma have been the subject of a wide array of research including paleoecology, physiology, morphological evolution, systematics, speciation, and hybridization. In recent years, much work has been done to elucidate evolutionary relationships within and between closely related species of the genus; in particular the addition of newly collected specimens from critical geographic regions has provided new opportunities for taxonomic assessment. Given these new data and their potential, parsimony (PARS), maximum likelihood (ML), and Bayesian inference (BI) analyses were conducted on DNA sequences obtained from nine individual genes (four mitochondrial loci: 12S, 16S, CoII, and Cytb; five nuclear loci: AdhI2, BfibI7, En2, Mlr, and Myh6) to estimate the phylogenetic relationships among 23 species of Neotoma. Results of these analyses depicted a wide array of phylogenetic relationships among taxa; with substantial nodal support recovered in both the ML and PARS analyses at some mid-level and terminal positions. Several individual genes, particularly 12S, AdhI2, BfibI7, CoII, and Cytb, provided support at several basal positions; however, phylogenetic resolution was limited in the other genes. A final BI analysis where the nine genes were concatenated into a single data set produced several supported clades that corresponded to previously recognized species groups (floridana, micropus, mexicana, and lepida) and the subgenus Homodontomys. Levels of genetic divergence for within-species comparisons (estimated from the Cytb data set) ranged from 0.88% (N. magister) to 6.82% (N. fuscipes); for between sister species comparisons ranged from 4.68% (N. devia and N. lepida) to 12.70% (N. angustapalata and N. nelsoni); and for members within closely related clades ranged from 8.70% (N. bryanti and N. lepida) to 12.57% (N. goldmani and N. magister). Evaluations of generic, subgeneric, and species group boundaries were explored using phylogenetic principles on the DNA sequence data presented herein, as well as morphological findings from previous studies. Results obtained suggest that the most conservative taxonomic interpretation involves the abandonment of subgeneric delineations and relies on the recognition of eight species groups (cinerea, floridana, fuscipes, lepida, mexicana, micropus, phenax, and stephensi) as the backbone of the woodrat classification.

Las ratas cambalacheras del género Neotoma han sido estudiadas en varios tipos de investigaciones incluyendo paleoecología, fisiología, evolución morfológica, sistemática, especiación e hibridación. Recientemente, se han realizado numerosos estudios para elucidar las relaciones evolutivas dentro del género y entre especies cercanamente relacionadas al mismo; en particular la inclusión de nuevos especímenes provenientes de regiones geográficas críticas han brindado nuevas oportunidades para evaluaciones taxonómicas. A partir de estos nuevos datos se realizaron análisis de parsimonia (PARS), Máxima Verosimilitud (MV), e Inferencia Bayesiana (IB) en secuencias de ADN provenientes de nueve genes individuales (cuatro loci mitocondriales: 12S, 16S, CoII, y Cytb; cinco loci nucleares: Adh-I2, Bfib-I7, En2, Mlr, and Myh6) para determinar la relación filogenética de 23 especies de Neotoma. Los resultados de estos análisis presentan una amplia gama de relaciones filogenéticas entre taxa con un soporte nodal importante en los análisis de MV y PARS en algunas posiciones terminales de nivel medio. Varios genes individuales, en particular 12S, Adh-I2, Bfib-I7, CoII, and Cytb, ofrecieron soporte en varias posiciones basales; sin embargo, la resolución filogenética fue reducida en los demás genes. El último análisis de IB, en donde nueve genes se concatenaron en un solo conjunto de datos, produjo soporte en varios clados que correspondieron a especies de grupos previamente reconocidos (floridana, micropus, mexicana, y lepida) y el sub-género Homodontomys. Los niveles de divergencia genética para comparaciones intraespecíficas fluctuaron entre 0.88% (N. magister) y 6.82% (N. fuscipes); para especies hermanas (4.68%­N. devia y N. lepida hasta 12.70%­N. angustapalata y N. nelsoni); y para los miembros de clados cercanos (8.70%­N. bryanti y N. lepida hasta 12.57%­N. goldmani y N. magister). Las evaluaciones de los limites genéricos, subgenéricos y de grupos de especies fueron explorados usando principios filogenéticos en las secuencias de ADN de este trabajo, y también se basaron en las conclusiones morfológicas de estudios previos. Los resultados obtenidos sugieren que la interpretación taxonómica más conservadora incluye el abandono de las delineaciones subgenéricas y se depende en el reconocimiento de ocho grupos de especies (cinerea, floridana, fuscipes, lepida, mexicana, micropus, phenax, y stephensi) como el pilar central de la clasificación de las ratas cambalacheras.

Trio-binned genomes of the woodrats Neotoma bryanti and Neotoma lepida reveal novel gene islands and rapid copy number evolution of xenobiotic metabolizing genes.

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.

The relevance of pedigrees in the conservation genomics era.

Over the past 50 years conservation genetics has developed a substantive toolbox to inform species management. One of the most long-standing tools available to manage genetics-the pedigree-has been widely used to characterize diversity and maximize evolutionary potential in threatened populations. Now, with the ability to use high throughput sequencing to estimate relatedness, inbreeding, and genome-wide functional diversity, some have asked whether it is warranted for conservation biologists to continue collecting and collating pedigrees for species management. In this perspective, we argue that pedigrees remain a relevant tool, and when combined with genomic data, create an invaluable resource for conservation genomic management. Genomic data can address pedigree pitfalls (e.g., founder relatedness, missing data, uncertainty), and in return robust pedigrees allow for more nuanced research design, including well-informed sampling strategies and quantitative analyses (e.g., heritability, linkage) to better inform genomic inquiry. We further contend that building and maintaining pedigrees provides an opportunity to strengthen trusted relationships among conservation researchers, practitioners, Indigenous Peoples, and Local Communities.

Toxin tolerance across landscapes: Ecological exposure not a prerequisite.

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 feces and quantified their tolerance to creosote bush through feeding trials using chow amended with creosote resin.Toxin tolerance was analyzed 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 greater than 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 kilometers 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.

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

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 F1 individuals 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.

Adaptive divergence despite low effective population size in a peripherally isolated population of the pygmy rabbit, Brachylagus idahoensis.

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.

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

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 bryanti and N. 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, parental N. bryanti and N. 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, with Frangula californica (California coffeeberry) making up a large portion of its diet. Neotoma lepida maintains a less diverse diet, with Prunus fasciculata (desert almond) comprising more than half of its diet. Both F. californica and P. 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 and N. lepida consumed F. californica and P. fasciculata, respectively, in greater abundance than these plants are available on the landscape-indicating dietary selection. Finally, experimental preference trials revealed that N. bryanti exhibited a preference for F. californica, while N. lepida exhibited a relatively stronger preference for P. fasciculata. We find that N. bryanti exhibit a generalist herbivore strategy relative to N. 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.

Lost in a sagebrush sea: comparative genetic assessment of an isolated montane population of Tamias amoenus.

The montane sky islands of the Great Basin are characterized by unique, isolated habitats and communities that likely are vulnerable to extirpation with environmental change. A subspecies of yellow pine chipmunk, the Humboldt yellow pine chipmunk (Tamias amoenus celeris), is associated with the whitebark and limber pine forests of the Pine Forest Range (PFR) in Nevada. We sampled T. amoenus and least chipmunks (T. minimus) from the isolated PFR and compared genetic diversity between these populations and more "mainland" populations, including other subspecies of chipmunks. Given the high frequency of hybridization in Tamias, we tested for hybridization between T. amoenus and T. minimus in the PFR. We examined phylogenetic relationships, population divergence and diversity, and screened populations for a common pathogen, Borrelia hermsii, to gain insight into population health. We found T. amoenus of the PFR are closely related to T. amoenus in the Warner Mountains and Sierra Nevada, but maintain substantively lower genetic variation. Microsatellite analyses show PFR T. amoenus are highly genetically differentiated from other populations. In contrast, PFR T. minimus had higher genetic diversity that was comparable to the other T. minimus population we sampled. Pathogen screening revealed that T. amoenus carried higher pathogen loads than T. minimus in the PFR, although the prevalence of infection was similar to other Tamias populations. Our assessment of habitat associations suggests that the Humboldt yellow pine chipmunk almost entirely is restricted to the conifer systems of the PFR, while least chipmunks are prevalent in the other forests. Our work highlights the need for continued conservation and research efforts to identify how response to environmental change can be facilitated in isolated species and habitats.

Genome-wide genetic variation coupled with demographic and ecological niche modeling of the dusky-footed woodrat (Neotoma fuscipes) reveal patterns of deep divergence and widespread Holocene expansion across northern California.

Understanding how species have responded to past climate change may help refine projections of how species and biotic communities will respond to future change. Here, we integrate estimates of genome-wide genetic variation with demographic and niche modeling to investigate the historical biogeography of an important ecological engineer: the dusky-footed woodrat, Neotoma fuscipes. We use RADseq to generate a genome-wide dataset for 71 individuals from across the geographic distribution of the species in California. We estimate population structure using several model-based methods and infer the demographic history of regional populations using a site frequency spectrum-based approach. Additionally, we use ecological niche modeling to infer current and past (Last Glacial Maximum) environmental suitability across the species' distribution. Finally, we estimate the directionality and possible spatial origins of regional population expansions. Our analyses indicate this species is subdivided into three regionally distinct populations, with the deepest divergence occurring ~1.7 million years ago across the modern-day San Francisco-Bay Delta region; a common biogeographic barrier for the flora and fauna of California. Our models of environmental suitability through time coincide with our estimates of population expansion, with relative long-term stability in the southern portion of the range, and more recent expansion into the northern end of the range. Our study illustrates how the integration of genome-wide data with spatial and demographic modeling can reveal the timing and spatial extent of historic events that determine patterns of biotic diversity and may help predict biotic response to future change.

The genetic legacy of 50 years of desert bighorn sheep translocations.

Conservation biologists have increasingly used translocations to mitigate population declines and restore locally extirpated populations. Genetic data can guide the selection of source populations for translocations and help evaluate restoration success. Bighorn sheep (Ovis canadensis) are a managed big game species that suffered widespread population extirpations across western North America throughout the early 1900s. Subsequent translocation programs have successfully re-established many formally extirpated bighorn herds, but most of these programs pre-date genetically informed management practices. The state of Nevada presents a particularly well-documented case of decline followed by restoration of extirpated herds. Desert bighorn sheep (O. c. nelsoni) populations declined to less than 3,000 individuals restricted to remnant herds in the Mojave Desert and a few locations in the Great Basin Desert. Beginning in 1968, the Nevada Department of Wildlife translocated ~2,000 individuals from remnant populations to restore previously extirpated areas, possibly establishing herds with mixed ancestries. Here, we examined genetic diversity and structure among remnant herds and the genetic consequences of translocation from these herds using a genotyping-by-sequencing approach to genotype 17,095 loci in 303 desert bighorn sheep. We found a signal of population genetic structure among remnant Mojave Desert populations, even across geographically proximate mountain ranges. Further, we found evidence of a genetically distinct, potential relict herd from a previously hypothesized Great Basin lineage of desert bighorn sheep. The genetic structure of source herds was clearly reflected in translocated populations. In most cases, herds retained genetic evidence of multiple translocation events and subsequent admixture when founded from multiple remnant source herds. Our results add to a growing literature on how population genomic data can be used to guide and monitor restoration programs.

Differential Effects of Climate on Survival Rates Drive Hybrid Zone Movement.

Climate change has been implicated as driving shifts of hybridizing species' range limits [1, 2]. Whether and how much hybrid zones move depends on the relative fitness of hybridzing species under changing conditions [3, 4]. However, fitness is rarely linked to both climatic conditions and movement of hybrid zones, such that the relationship between climate change and hybrid zone dynamics remains tenuous [5]. Here we report how interactions between climate (seasonal precipitation) and competitor densities result in steep differentials in survival, which in turn drive hybrid zone movement for two woodrat species (Neotoma fuscipes and N. macrotis) in central California, USA. Using 6 years of capture-mark-recapture data, we found that the smaller-bodied species, N. macrotis, and hybrids had survival advantages over the larger-bodied N. fuscipes in the contact region during dry winters and wet springs. This pattern of differential survival, with N. macrotis having a consistent advantage over N. fuscipes during our study period, matched the spatial dynamics of the hybrid zone, which moved steadily north into N. fuscipes territory, with its estimated center moving ∼150 m north in 6 years. Our findings provide a unique demonstration of range movements emerging from a complex interplay between climate and competition. Although all study site areas experienced the same climatic conditions, competitive effects created a complex spatial pattern of survival differentials, which in turn influenced hybrid zone movement. Characterization of fitness differentials derived from replicated demographic studies of contact regions between competitors should greatly improve our ability to understand and forecast climate-driven range dynamics.

Biodiversity and Topographic Complexity: Modern and Geohistorical Perspectives.

Topographically complex regions on land and in the oceans feature hotspots of biodiversity that reflect geological influences on ecological and evolutionary processes. Over geologic time, topographic diversity gradients wax and wane over millions of years, tracking tectonic or climatic history. Topographic diversity gradients from the present day and the past can result from the generation of species by vicariance or from the accumulation of species from dispersal into a region with strong environmental gradients. Biological and geological approaches must be integrated to test alternative models of diversification along topographic gradients. Reciprocal illumination among phylogenetic, phylogeographic, ecological, paleontological, tectonic, and climatic perspectives is an emerging frontier of biogeographic research.

Multiscale connectivity and graph theory highlight critical areas for conservation under climate change.

Conservation planning and biodiversity management require information on landscape connectivity across a range of spatial scales from individual home ranges to large regions. Reduction in landscape connectivity due changes in land use or development is expected to act synergistically with alterations to habitat mosaic configuration arising from climate change. We illustrate a multiscale connectivity framework to aid habitat conservation prioritization in the context of changing land use and climate. Our approach, which builds upon the strengths of multiple landscape connectivity methods, including graph theory, circuit theory, and least-cost path analysis, is here applied to the conservation planning requirements of the Mohave ground squirrel. The distribution of this threatened Californian species, as for numerous other desert species, overlaps with the proposed placement of several utility-scale renewable energy developments in the American southwest. Our approach uses information derived at three spatial scales to forecast potential changes in habitat connectivity under various scenarios of energy development and climate change. By disentangling the potential effects of habitat loss and fragmentation across multiple scales, we identify priority conservation areas for both core habitat and critical corridor or stepping stone habitats. This approach is a first step toward applying graph theory to analyze habitat connectivity for species with continuously distributed habitat and should be applicable across a broad range of taxa.

Speciation along a shared evolutionary trajectory.

Groups of organisms-whether multiple species or populations of a single species-can differ in several non-exclusive ways. For example, groups may have diverged phenotypically, genetically, or in the evolutionary responses available to them. We tested for the latter of these-response divergence-between 2 species of woodrats: Neotoma fuscipes and Neotoma macrotis. Based on random skewers analyses we found that, despite being well differentiated both phenotypically and genetically, N. fuscipes and N. macrotis appear to be diverging along a shared evolutionary trajectory (r° = 0.895, P = 0.114). Because these species are currently in secondary contact, their phenotypic evolution being along a shared evolutionary axis has important implications. In particular, that their response to selection arising from interspecific interactions will be constrained along the same evolutionary trajectory may reduce the potential for reinforcing selection to maintain species boundaries.

Parasite prevalence and community diversity in sympatric and allopatric populations of two woodrat species (Sigmodontinae: Neotoma) in central California.

Patterns of host-parasite association may vary across the landscape in part because of host and parasite diversity, divergence, local ecology, or interactions among these factors. In central coastal California, we quantified parasite prevalence, infection intensity, and diversity in two sister species of woodrats (Neotoma fuscipes and Neotoma macrotis) where the species co-occur (sympatry) and where each species exists alone (allopatry). In feces from 50 adults we identified seven taxa: the protozoans Eimeria, Giardia, and Cryptosporidium, the nematodes Trichuris, Aspicularis, and Eucoleus, and a cestode in the family Anoplocephalidae. Gastrointestinal parasite infection intensity and diversity were higher in males than in females, a difference that was most pronounced in the more aggressive N. fuscipes. Both species had lower infection intensity in sympatry than in allopatry and in sympatry the two species did not differ in infection intensity in total but did maintain distinct parasite communities. Taken together, our findings suggest that host evolutionary differences, including perhaps species-specific patterns of aggressive behavior, as well as local ecology, influence the likelihood of infection by these endoparasite taxa.

Ecological segregation in a small mammal hybrid zone: habitat-specific mating opportunities and selection against hybrids restrict gene flow on a fine spatial scale.

The degree to which closely related species interbreed is determined by a complex interaction of ecological, behavioral, and genetic factors. We examine the degree of interbreeding between two woodrat species, Neotoma bryanti and N. lepida, at a sharp ecological transition. We identify the ecological association of each genotypic class, assess the opportunity for mating between these groups, and test whether they have similar patterns of year-to-year persistence on our study site. We find that 13% of individuals have a hybrid signature but that the two parental populations and backcrosses are highly segregated by habitat type and use. Also, we find that adult hybrids are comparable to parental types in terms of year-to-year persistence on our site but that, among juveniles, significantly fewer hybrids reach adulthood on site compared to their purebred counterparts. Our analyses show that this hybrid zone is maintained by occasional nonassortative mating coupled with hybrid fertility, but that these factors are balanced by lower apparent survival of juvenile hybrids and habitat-based preference or selection that limits heterospecific mating while promoting backcrossing to habitat-specific genotypes. This system presents a novel example of the role that sharp resource gradients play in reproductive isolation and the potential for genetic introgression.