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Variation and differentiation among populations provide a framework to decipher how populations are, or are not, changing due to gene flow, genetic drift, and selection. The sagebrush least chipmunk (Tamias minimus scrutator) is distributed in arid and semi-arid habitats throughout much of the Great Basin and adjacent regions. The broad distribution and variation in elevation of populations make this a good system to assess population variation and the forces shaping differentiation. Here, we use allozyme and morphological datasets to: 1) assess the relative roles of geographic locality and elevation of populations in shaping population structure; 2) examine the level of differentiation of peripheral and isolated populations; and 3) compare the genetic and morphological signals of population variation and structure. We sampled 312 individuals from 12 T. minimus scrutator populations and other areas of their distribution. Individuals were measured for 27 genetic and 61 morphological traits. These datasets were analyzed to determine the distribution of variation and the differentiation among populations and tested for correlations with geographic distance and elevation. Multiple approaches were used to thoroughly compare the signals from each dataset. We found 13 polymorphic electrophoretic loci with most of the variation structured among populations within regions. Eight loci exhibited elevational heterogeneity but most high-elevation populations showed no heterogeneity among populations. Thirty-two morphological characters varied among populations but with no discernable trends across regions or elevations. Populations had varying levels of asymmetric distinctness in morphological characters, but there were no significant differences among populations. Morphological and genetic distance measures were correlated and there was some evidence of a correlation of genetic and geographic distance. We also found some correlation of asymmetric distances with morphological or genetic distances at smaller scales. There was substantial variation of genetic and morphological traits among sagebrush least chipmunk populations. Each population had a unique genetic signature and significant morphological differentiation. Our results suggest that genetic drift is contributing to the structure of these populations, with some evidence of selection shaping the distribution of variation at different elevations. The peripheral populations had mixed signals of isolation among the different datasets, with an overall signature suggesting that genetic drift is also driving the variation among these populations. The different measures of population variation yielded inconsistent signals of population structure, highlighting the need for multiple approaches to assess population variation. The variation among sagebrush least chipmunk populations is impacted by a variety of factors and contemporary investigations may reveal populations responding to alterations in habitat and climate.

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.

Urban environments are among the fastest changing habitats on the planet, and this change has evolutionary implications for the organisms inhabiting them. Herein, we demonstrate that natural history collections are critical resources for urban evolution studies. The specimens housed in these collections provide great potential for diverse types of urban evolution research, and strategic deposition of specimens and other materials from contemporary studies will determine the resources and research questions available to future urban evolutionary biologists. As natural history collections are windows into the past, they provide a crucial historical timescale for urban evolution research. While the importance of museum collections for research is generally appreciated, their utility in the study of urban evolution has not been explicitly evaluated. Here, we: (a) demonstrate that museum collections can greatly enhance urban evolution studies, (b) review patterns of specimen use and deposition in the urban evolution literature, (c) analyze how urban versus rural and native versus nonnative vertebrate species are being deposited in museum collections, and (d) make recommendations to researchers, museum professionals, scientific journal editors, funding agencies, permitting agencies, and professional societies to improve archiving policies. Our analyses of recent urban evolution studies reveal that museum specimens can be used for diverse research questions, but they are used infrequently. Further, although nearly all studies we analyzed generated resources that could be deposited in natural history collections (e.g., collected specimens), a minority (12%) of studies actually did so. Depositing such resources in collections is crucial to allow the scientific community to verify, replicate, and/or re‐visit prior research. Therefore, to ensure that adequate museum resources are available for future urban evolutionary biology research, the research community—from practicing biologists to funding agencies and professional societies—must make adjustments that prioritize the collection and deposition of urban specimens.

Discovery of cryptic species is essential to understanding the process of speciation and assessing the impacts of anthropogenic stressors. Here, we used genomic data to test for cryptic species diversity within an ecologically well-known radiation of North American rodents, western chipmunks (Tamias). We assembled a de novo reference genome for a single species (Tamias minimus) combined with new and published targeted sequence-capture data for 21,551 autosomal and 493 X-linked loci sampled from 121 individuals spanning 22 species. We identified at least two cryptic lineages corresponding with an isolated subspecies of least chipmunk (T. minimus grisescens) and with a restricted subspecies of the yellow-pine chipmunk (T. amoenus cratericus) known only from around the extensive Craters of the Moon lava flow. Additional population-level sequence data revealed that the so-called Crater chipmunk is a distinct species that is abundant throughout the coniferous forests of southern Idaho. This cryptic lineage does not appear to be most closely related to the ecologically and phenotypically similar yellow-pine chipmunk but does show evidence for recurrent hybridization with this and other species.

Museum specimens play an increasingly important role in predicting the outcomes and revealing the consequences of anthropogenically driven disruption of the biosphere. As ecological communities respond to ongoing environmental change, host–parasite interactions are also altered. This shifting landscape of host–parasite associations creates opportunities for colonization of different hosts and emergence of new pathogens, with implications for wildlife conservation and management, public health, and other societal concerns. Integrated archives that document and preserve mammal specimens along with their communities of associated parasites and ancillary data provide a powerful resource for investigating, anticipating, and mitigating the epidemiological, ecological, and evolutionary impacts of environmental perturbation. Mammalogists who collect and archive mammal specimens have a unique opportunity to expand the scope and impact of their field work by collecting the parasites that are associated with their study organisms. We encourage mammalogists to embrace an integrated and holistic sampling paradigm and advocate for this to become standard practice for museum-based collecting. To this end, we provide a detailed, field-tested protocol to give mammalogists the tools to collect and preserve host and parasite materials that are of high quality and suitable for a range of potential downstream analyses (e.g., genetic, morphological). Finally, we also encourage increased global cooperation across taxonomic disciplines to build an integrated series of baselines and snapshots of the changing biosphere. Los especímenes de museo desempeñan un papel cada vez más importante tanto en la descripción de los resultados de la alteración antropogénica de la biosfera como en la predicción de sus consecuencias. Dado que las comunidades ecológicas responden al cambio ambiental, también se alteran las interacciones hospedador-parásito. Este panorama cambiante de asociaciones hospedador-parásito crea oportunidades para la colonización de diferentes hospedadores y para la aparición de nuevos patógenos, con implicancias en la conservación y manejo de la vida silvestre, la salud pública y otras preocupaciones de importancia para la sociedad. Archivos integrados que documentan y preservan especímenes de mamíferos junto con sus comunidades de parásitos y datos asociados, proporcionan un fuerte recurso para investigar, anticipar y mitigar los impactos epidemiológicos, ecológicos y evolutivos de las perturbaciones ambientales. Los mastozoólogos que recolectan y archivan muestras de mamíferos, tienen una oportunidad única de ampliar el alcance e impacto de su trabajo de campo mediante la recolección de los parásitos que están asociados con los organismos que estudian. Alentamos a los mastozoólogos a adoptar un paradigma de muestreo integrado y holístico y abogamos para que esto se convierta en una práctica estándarizada de la obtención de muestras para museos. Con este objetivo, proporcionamos un protocolo detallado y probado en el campo para brindar a los mastozoólogos las herramientas para recolectar y preservar materiales de parásitos y hospedadores de alta calidad y adecuados para una gran variedad de análisis subsecuentes (e.g., genéticos, morfológicos, etc.). Finalmente, también abogamos por una mayor cooperación global entre las diversas disciplinas taxonómicas para construir una serie integrada de líneas de base y registros actuales de nuestra cambiante biosfera.

Phylosymbiosis refers to a congruent pattern between the similarity of microbiomes of different species and the branching pattern of the host phylogeny. Phylosymbiosis has been detected in a variety of vertebrate and invertebrate hosts, but has only been assessed in geographically isolated populations. We tested for phylosymbiosis in eight (sub)species of western chipmunks with overlapping ranges and ecological niches; we used a nuclear (Acrosin) and a mitochondrial (CYTB) phylogenetic marker because there are many instances of mitochondrial introgression in chipmunks. We predicted that similarity among microbiomes increases with: (1) increasing host mitochondrial relatedness, (2) increasing host nuclear genome relatedness and (3) decreasing geographic distance among hosts. We did not find statistical evidence supporting phylosymbiosis in western chipmunks. Furthermore, in contrast to studies of other mammalian microbiomes, similarity of chipmunk microbiomes is not predominantly determined by host species. Sampling site explained most variation in microbiome composition, indicating an important role of local environment in shaping microbiomes. Fecal microbiomes of chipmunks were dominated by Bacteroidetes (72.2%), followed by Firmicutes (24.5%), which is one of the highest abundances of Bacteroidetes detected in wild mammals. Future work will need to elucidate the effects of habitat, ecology and host genomics on chipmunk microbiomes.

Climate and host demographic cycling often shape both parasite genetic diversity and host distributions, processes that transcend a history of strict host–parasite association. We explored host associations and histories based on an evaluation of mitochondrial and nuclear sequences to reveal the underlying history and genetic structure of a pinworm, Rauschtineria eutamii, infecting ten species of western North American chipmunks (Rodentia:Tamias, subgenus Neotamias). Rauschtineria eutamii contains divergent lineages influenced by the diversity of hosts and variation across the complex topography of western North America. We recovered six reciprocally monophyletic R. eutamii mitochondrial clades, largely supported by a multilocus concordance tree, exhibiting divergence levels comparable with intraspecific variation reported for other nematodes. Phylogenetic relationships among pinworm clades suggest that R. eutamii colonized an ancestral lineage of western chipmunks and lineages persisted during historical isolation in diverging Neotamias species or species groups. Pinworm diversification, however, is incongruent and asynchronous relative to host diversification. Secondarily, patterns of shallow divergence were shaped by geography through events of episodic colonization reflecting an interaction of taxon pulses and ecological fitting among assemblages in recurrent sympatry. Pinworms occasionally infect geographically proximal host species; however, host switching may be unstable or ephemeral, as there is no signal of host switching in the deeper history of R. eutamii.

Found throughout the tree of life and in every ecosystem, parasites are some of the most diverse, ecologically important animals on Earth-but in almost all cases, the least protected by wildlife or ecosystem conservation efforts. For decades, ecologists have been calling for research to understand parasites' important ecological role, and increasingly, to protect as many species from extinction as possible. However, most conservationists still work within priority systems for funding and effort that exclude or ignore parasites, or treat parasites as an obstacle to be overcome. Our working group identified 12 goals for the next decade that could advance parasite biodiversity conservation through an ambitious mix of research, advocacy, and management. Ecological Society of America; Georgetown Environment Initiative; Smithsonian National Museum of Natural HistorySmithsonian InstitutionSmithsonian National Museum of Natural History; Peter Buck Postdoctoral Fellowship from the Smithsonian National Museum of Natural History; National Science FoundationNational Science Foundation (NSF) [OCE-1829509]; Alfred P. Sloan Foundation Sloan Research FellowshipAlfred P. Sloan Foundation; University of Washington Innovation Award; University of Washington Royalty Research Fund awardUniversity of Washington The authors kindly thank the Ecological Society of America for supporting our workshop, as well as additional participants Kevin Burgio, Tad Dallas, and Roger Jovani; Laura Whitehouse, for her graphic design work on Fig. 1; Jonathan Wojcik for allowing the inclusion of his copyright Diplozoon illustration in Fig. 3; and dozens of collaborators and friends who have been part of the foundational work on parasite conservation, including Anna Phillips, Veronica Bueno, Carrie Cizauskas, Christopher Clements, Graeme Cumming, Eric Dougherty, Kevin Johnson, Wayne Getz, Nyeema Harris, Elizabeth Nichols, Sergey Mironov, Robert Poulin, and Heather Proctor. CJC gratefully acknowledges funding support from the Georgetown Environment Initiative, and research support from Anna Phillips and the Smithsonian National Museum of Natural History. KCB was supported by a Peter Buck Postdoctoral Fellowship from the Smithsonian National Museum of Natural History. CLW was supported by a grant from the National Science Foundation (OCE-1829509), an Alfred P. Sloan Foundation Sloan Research Fellowship, a University of Washington Innovation Award, and a University of Washington Royalty Research Fund award. Any use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the U.S. Government. Public domain – authored by a U.S. government employee

Preparing students to explore, understand, and resolve societal challenges such as global climate change is an important task for evolutionary and ecological biologists that will require novel and innovative pedagogical approaches. Recent calls to reform undergraduate science education emphasize the importance of engaging students in inquiry-driven, active, and authentic learning experiences. We believe that the vast digital resources (i.e., “big data”) associated with natural history collections provide invaluable but underutilized opportunities to create such experiences for undergraduates in biology. Here, we describe an online, open-access educational module that we have developed that harnesses the power of collections-based information to introduce students to multiple conceptual and analytical elements of climate change, evolutionary, and ecological biology research. The module builds upon natural history specimens and data collected over the span of nearly a century in Yosemite National Park, California, to guide students through a series of exercises aimed at testing hypotheses regarding observed differences in response to climate change by two closely related and partially co-occurring species of chipmunks. The content of the module can readily be modified to meet the pedagogical goals and instructional levels of different courses while the analytical strategies outlined can be adapted to address a wide array of questions in evolutionary and ecological biology. In sum, we believe that specimen-based natural history data represent a powerful platform for reforming undergraduate instruction in biology. Because these efforts will result in citizens who are better prepared to understand complex biological relationships, the benefits of this approach to undergraduate education will have widespread benefits to society.

There is an emerging consensus that undergraduate biology education in the United States is at a crucial juncture, especially as we acknowledge the need to train a new generation of scientists to meet looming environmental and health crises. Digital resources for biology now available online provide an opportunity to transform biology curricula to include more authentic and inquiry-driven educational experiences. Digitized natural history collections have become tremendous assets for research in environmental and health sciences, but, to date, these data remain largely untapped by educators. Natural history collections have the potential to help transform undergraduate science education from passive learning into an active exploration of the natural world, including the exploration of the complex relationships among environmental conditions, biodiversity, and human well-being. By incorporating natural history specimens and their associated data into undergraduate curricula, educators can promote participatory learning and foster an understanding of essential interactions between organisms and their environments.Keywords: databases, inquiry driven, museum, place based, undergraduate education

Phylogenomic data sets are illuminating many areas of the Tree of Life. However, the large size of these data sets alone may be insufficient to resolve problematic nodes in the most rapid evolutionary radiations, because inferences in zones of extraordinarily low phylogenetic signal can be sensitive to the model and method of inference, as well as the information content of loci employed. We used a data set of $>$3950 ultraconserved element (UCE) loci from a classic mammalian radiation, ground-dwelling squirrels of the tribe Marmotini (Sciuridae: Xerinae), to assess sensitivity of phylogenetic estimates to varying per-locus information content across four different inference methods (RAxML, ASTRAL, NJst, and SVDquartets). Persistent discordance was found in topology and bootstrap support between concatenation- and coalescent-based inferences; among methods within the coalescent framework; and within all methods in response to different filtering scenarios. Contrary to some recent empirical UCE-based studies, filtering by information content did not promote complete among-method concordance. Nevertheless, filtering did improve concordance relative to randomly selected locus sets, largely via improved consistency of two-step summary methods (particularly NJst) under conditions of higher average per-locus variation (and thus increasing gene tree precision). The benefits of phylogenomic data set filtering are variable among classes of inference methods and across different evolutionary scenarios, reiterating the complexities of resolving rapid radiations, even with robust taxon and character sampling.

Climate and host demographic cycling often shape both parasite genetic diversity and host distributions, processes that transcend a history of strict host-parasite association. We explored host associations and histories based on an evaluation of mitochondrial and nuclear sequences to reveal the underlying history and genetic structure of a pinworm, Rauschtineria eutamii, infecting 10 species of western North American chipmunks (Rodentia:Tamias, subgenus Neotamias). Rauschtineria eutamii contains divergent lineages influenced by the diversity of hosts and variation across the complex topography of western North America. We recovered six reciprocally monophyletic R. eutamii mitochondrial clades, largely supported by nuclear gene trees, exhibiting divergence levels comparable to intraspecific variation reported for other nematodes. Phylogenetic relationships among pinworm clades suggest that R. eutamii colonized an ancestral lineage of western chipmunks and lineages persisted during historical isolation in diverging Neotamias species or species groups. Pinworm diversification, however, is incongruent and asynchronous relative to host diversification. Secondarily, patterns of shallow divergence were shaped by geography through events of episodic colonization reflecting an interaction of taxon pulses and ecological fitting among assemblages in recurrent sympatry. Pinworms occasionally infect geographically proximal host species; however, host switching may be unstable or ephemeral, as there is no signal of host switching in the deeper history of R. eutamii.

Aim The Mohave ground squirrel (Xerospermophilus mohavensis) is one of a few endemic species of the Mojave Desert of south-western North America. We describe phylogeographic patterns within this species and its sister taxon (Xerospermophilus tereticaudus) and test hypotheses concerning their biogeographical history using genetic signatures of stable versus expanding populations. We compare these patterns with those of other Mojave species to evaluate the role of vicariance in producing phylogeographic structure during the assembly of the Mojave Desert biota. Location The Mojave Desert and adjacent desert regions of south-western North America. Methods Complete cytochrome b gene sequences of X. mohavensis (46 individuals representing 11 localities) and X. tereticaudus (38 individuals representing 14 localities) were analysed using Bayesian methods to infer phylogenetic relationships. Genetic signals of stable or expanding populations were examined based on the distribution of recent mutations and pairwise differences, as well as with a coalescent-based approach. Results The two species are reciprocally monophyletic and may have diverged in response to the late Pliocene–early Pleistocene uplift of the Transverse Ranges and Mojave block. Little phylogeographic structure is evident within X. mohavensis, but there is a signature of northern expansion from a presumably full-pluvial refugium in the Mojave River basin. Four geographic subgroups are evident within X. tereticaudus, and there is a signature of northern expansion from a presumably full-pluvial refugium in the Sonoran coastal plains. Roughly congruent phylogeographic patterns are found within five arid-adapted taxa, indicating a strong element of vicariance during the assembly of the generally transitional Mojave Desert biota. Main conclusions We present a preliminary model for the historical assembly of the Mojave Desert biota that indicates a strong vicariant element producing autochthonous lineages (including X. mohavensis) that diverged during the major geological and climatic events of the last 5 Myr. Phylogeographic partitioning within the Mojave Desert underscores the necessity of immediate conservation measures for this unique and fragile arid ecosystem that is locked between two large metropolitan population centres and is the target of continued adverse environmental impact.

Specimens and associated data in natural history collections (NHCs) foster substantial scientific progress. In this paper, we explore recent contributions of NHCs to the study of systematics and biogeography, genomics, morphology, stable isotope ecology, and parasites and pathogens of mammals. To begin to assess the magnitude and scope of these contributions, we analyzed publications in the Journal of Mammalogy over the last decade, as well as recent research supported by a single university mammal collection (Museum of Southwestern Biology, Division of Mammals). Using these datasets, we also identify weak links that may be hindering the development of crucial NHC infrastructure. Maintaining the vitality and growth of this foundation of mammalogy depends on broader engagement and support from across the scientific community and is both an ethical and scientific imperative given the rapidly changing environmental conditions on our planet.

Increasing data have supported the importance of divergence with gene flow (DGF) in the generation of biological diversity. In such cases, lineage divergence occurs on a shorter timescale than does the completion of reproductive isolation. Although it is critical to explore the mechanisms driving divergence and preventing homogenization by hybridization, it is equally important to document cases of DGF in nature. Here we synthesize data that have accumulated over the last dozen or so years on DGF in the chipmunk (Tamias) radiation with new data that quantify very high rates of mitochondrial DNA (mtDNA) introgression among para- and sympatric species in the T. quadrivittatus group in the central and southern Rocky Mountains. These new data (188 cytochrome b sequences) bring the total number of sequences up to 1871; roughly 16% (298) of the chipmunks we have sequenced exhibit introgressed mtDNA. This includes ongoing introgression between subspecies and between both closely related and distantly related taxa. In addition, we have identified several taxa that are apparently fixed for ancient introgressions and in which there is no evidence of ongoing introgression. A recurrent observation is that these introgressions occur between ecologically and morphologically diverged, sometimes non-sister taxa that engage in well-documented niche partitioning. Thus, the chipmunk radiation in western North America represents an excellent mammalian example of speciation in the face of recurrent gene flow among lineages and where biogeography, habitat differentiation and mating systems suggest important roles for both ecological and sexual selection.

Novel sequencing technologies are rapidly expanding the size of data sets that can be applied to phylogenetic studies. Currently the most commonly used phylogenomic approaches involve some form of genome reduction. While these approaches make assembling phylogenomic data sets more economical for organisms with large genomes, they reduce the genomic coverage and thereby the long-term utility of the data. Currently, for organisms with moderate to small genomes (< 1000 Mbp) it is feasible to sequence the entire genome at modest coverage (10−30×). Computational challenges for handling these large data sets can be alleviated by assembling targeted reads, rather than assembling the entire genome, to produce a phylogenomic data matrix. Here we demonstrate the use of automated Target Restricted Assembly Method (aTRAM) to assemble 1107 single-copy ortholog genes from whole genome sequencing of sucking lice (Anoplura) and out-groups. We developed a pipeline to extract exon sequences from the aTRAM assemblies by annotating them with respect to the original target protein. We aligned these protein sequences with the inferred amino acids and then performed phylogenetic analyses on both the concatenated matrix of genes and on each gene separately in a coalescent analysis. Finally, we tested the limits of successful assembly in aTRAM by assembling 100 genes from close- to distantly related taxa at high to low levels of coverage. Both the concatenated analysis and the coalescent-based analysis produced the same tree topology, which was consistent with previously published results and resolved weakly supported nodes. These results demonstrate that this approach is successful at developing phylogenomic data sets from raw genome sequencing reads. Further, we found that with coverages above 5−10× , aTRAM was successful at assembling 80–90% of the contigs for both close and distantly related taxa. As sequencing costs continue to decline, we expect full genome sequencing will become more feasible for a wider array of organisms, and aTRAM will enable mining of these genomic data sets for an extensive variety of applications, including phylogenomics. [aTRAM; gene assembly; genome sequencing; phylogenomics.] Fil: Allen, Julie M.. University of Illinois at Urbana-Champaign; Estados Unidos Fil: Boyd, Christopher. University of Illinois at Urbana-Champaign; Estados Unidos Fil: Nguyen, Nam Phuong. University of Illinois at Urbana-Champaign; Estados Unidos Fil: Vachaspati, Pranjal. University of Illinois at Urbana-Champaign; Estados Unidos Fil: Warnow, Tandy. University of Illinois at Urbana-Champaign; Estados Unidos Fil: Huang, Daisie I.. University of British Columbia; Canadá Fil: Grady, Patrick G. S.. University of Illinois at Urbana-Champaign; Estados Unidos Fil: Bell, Kayce C.. University Of New Mexico; Estados Unidos Fil: Cronk, Quentin C. B.. University of British Columbia; Canadá Fil: Mugisha, Lawrence. Makerere University; Uganda Fil: Pittendrigh, Barry R.. Michigan State University; Estados Unidos Fil: Leonardi, María Soledad. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Centro Nacional Patagónico. Instituto de Biología de Organismos Marinos; Argentina Fil: Reed, David L.. University of Florida; Estados Unidos Fil: Johnson, Kevin P.. University of Illinois at Urbana-Champaign; Estados Unidos