Seasonal and sex-specific changes in the gastrointestinal tracts of Peromyscus maniculatus.

Functional traits are phenotypic characteristics that contribute to fitness of individuals in dynamic and changing environments. In mammals, both categorical and continuous (e.g., quantitative) functional traits have been extensively utilized as proxies for diet, locomotion, and other aspects of species ecology, but there has been less focus on form and function of soft tissues. This is particularly true for the digestive system, which varies in size and complexity across Class Mammalia and plays a major role in the energetics of species. To guide more effective utilization of gastrointestinal (GI) morphology as a functional proxy in small mammal ecology, we examined how GI tracts (lengths and masses of four GI sections) varied within a population of deer mice (Peromyscus maniculatus) in the Southern Appalachian Mountains of North Carolina, United States. We collected samples of adult P. maniculatus monthly for 1 year and measured GI tracts to quantify variation with respect to seasonality and trophic level, providing insight into plasticity in this soft tissue trait over time. We found that season had a significant effect on the total length and wet mass of the GI tract, with January mice having the longest GI tracts and lengths being shortest in the summer. The relative shortening of the GI tract in summer corresponded with a partial trophic increase detected by stable isotope signatures. GI length and wet mass also were affected by reproduction, but males and females responded in sex-specific ways to demands of reproduction, with reproductively active males having shorter and lighter GI tracts than nonreproductively active males. Our study provides proof-of-concept for understanding population-level plasticity in a rarely collected soft tissue trait, which may also be complementary to standard craniodental measurements as a functional dietary proxy to understand mammalian ecology and community assembly.

Los rasgos funcionales son características fenotípicas que contribuyen a la aptitud de los individuos en entornos dinámicos y cambiantes. En los mamíferos, los rasgos funcionales categóricos y continuos (por ejemplo, cuantitativos) se han utilizado ampliamente como indicadores de la dieta, la locomoción y otros aspectos de la ecología de las especies, a la vez que se ha prestado menos atención a la forma y función de los tejidos blandos. Este es particularmente el caso del sistema digestivo, que varía en tamaño y complejidad a través de la Clase Mammalia, jugando un papel importante en la energética de las especies. Para propiciar una utilización más efectiva de la morfología gastrointestinal (GI) como un rasgo funcional en la ecología de los pequeños mamíferos, examinamos cómo los tractos GIs (longitudes y masas de cuatro secciones GI) variaban dentro de una población de ratones ciervos (Peromyscus maniculatus) de las Montañas Apalaches del sur de Carolina del Norte, Estados Unidos. Mensualmente, durante un año, recolectamos especímenes adultos de P. maniculatus y medimos sus tractos gastrointestinales para cuantificar la variación con respecto a la estacionalidad y el nivel trófico, brindando información sobre la plasticidad en estos rasgos de tejido blando a lo largo del tiempo. Descubrimos que la estacionalidad tiene un efecto significativo en la longitud total y la masa húmeda del tracto gastrointestinal, ya que los ratones de enero tienen los tractos gastrointestinales más largos y las longitudes son más cortas durante el verano. El acortamiento relativo del tracto GI en verano se correspondió con un aumento trófico parcial detectado por las cuantificación de isótopos estables. La longitud GI y la masa húmeda también se vieron afectadas por la reproducción; pero los machos y las hembras respondieron de manera diferente a las demandas de la reproducción. Los machos reproductivamente activos tienen tractos gastrointestinales más cortos y ligeros que los machos no activos reproductivamente. Nuestro estudio constituye un avance para comprender la plasticidad a nivel de población en un rasgo de tejido blando raramente recolectado, que también puede ser complementario a las mediciones craneodentales estándar como un proxy dietético funcional para entender la ecología de los mamíferos y el ensamblaje de la comunidad.

A solution to the challenges of interdisciplinary aggregation and use of specimen-level trait data.

Understanding variation of traits within and among species through time and across space is central to many questions in biology. Many resources assemble species-level trait data, but the data and metadata underlying those trait measurements are often not reported. Here, we introduce FuTRES (Functional Trait Resource for Environmental Studies; pronounced few-tress), an online datastore and community resource for individual-level trait reporting that utilizes a semantic framework. FuTRES already stores millions of trait measurements for paleobiological, zooarchaeological, and modern specimens, with a current focus on mammals. We compare dynamically derived extant mammal species' body size measurements in FuTRES with summary values from other compilations, highlighting potential issues with simply reporting a single mean estimate. We then show that individual-level data improve estimates of body mass-including uncertainty-for zooarchaeological specimens. FuTRES facilitates trait data integration and discoverability, accelerating new research agendas, especially scaling from intra- to interspecific trait variability.

Rickettsia felis and Other Rickettsia Species in Chigger Mites Collected from Wild Rodents in North Carolina, USA.

Chiggers are vectors of rickettsial pathogenic bacteria, Orientia spp., that cause the human disease, scrub typhus, in the Asian-Pacific area and northern Australia (known as the Tsutsugamushi Triangle). More recently, reports of scrub typhus in Africa, southern Chile, and the Middle East have reshaped our understanding of the epidemiology of this disease, indicating it has a broad geographical distribution. Despite the growing number of studies and discoveries of chigger-borne human disease outside of the Tsutsugamushi Triangle, rickettsial pathogens in chigger mites in the US are still undetermined. The aim of our study was to investigate possible Rickettsia DNA in chiggers collected from rodents in North Carolina, USA. Of 46 chiggers tested, 47.8% tested positive for amplicons of the 23S-5S gene, 36.9% tested positive for 17 kDa, and 15.2% tested positive for gltA. Nucleotide sequence analyses of the Rickettsia-specific 23S-5S intergenic spacer (IGS), 17 kDa, and gltA gene fragments indicated that the amplicons from these chiggers were closely related to those in R. felis, R. conorii, R. typhi, and unidentified Rickettsia species. In this study, we provide the first evidence of Rickettsia infection in chiggers collected from rodents within the continental USA. In North Carolina, a US state with the highest annual cases of spotted fever rickettsioses, these results suggest chigger bites could pose a risk to public health, warranting further study.

Old specimens for old branches: Assessing effects of sample age in resolving a rapid Neotropical radiation of squirrels.

Ultraconserved Elements (UCEs) have been useful to resolve challenging phylogenies of non-model clades, unpuzzling long-conflicted relationships in key branches of the Tree of Life at both deep and shallow levels. UCEs are often reliably recovered from historical samples, unlocking a vast number of preserved natural history specimens for analysis. However, the extent to which sample age and preservation method impact UCE recovery as well as downstream inferences remains unclear. Furthermore, there is an ongoing debate on how to curate, filter, and properly analyze UCE data when locus recovery is uneven across sample age and quality. In the present study we address these questions with an empirical dataset composed of over 3800 UCE loci from 219 historical and modern samples of Sciuridae, a globally distributed and ecologically important family of rodents. We provide a genome-scale phylogeny of two squirrel subfamilies (Sciurillinae and Sciurinae: Sciurini) and investigate their placement within Sciuridae. For historical specimens, recovery of UCE loci and mean length per locus were inversely related to sample age; deeper sequencing improved the number of UCE loci recovered but not locus length. Most of our phylogenetic inferences-performed on six datasets with alternative data-filtering strategies, and using three distinct optimality criteria-resulted in distinct topologies. Datasets containing more loci (40% and 50% taxa representativeness matrices) yielded more concordant topologies and higher support values than strictly filtered datasets (60% matrices) particularly with IQ-Tree and SVDquartets, while filtering based on information content provided better topological resolution for inferences with the coalescent gene-tree based approach in ASTRAL-III. We resolved deep relationships in Sciuridae (including among the five currently recognized subfamilies) and relationships among the deepest branches of Sciurini, but conflicting relationships remain at both genus- and species-levels for the rapid Neotropical tree squirrel radiation. Our results suggest that phylogenomic consensus can be difficult and heavily influenced by the age of available samples and the filtering steps used to optimize dataset properties.

SNP-based phylogenomic inference in Holarctic ground squirrels (Urocitellus).

Resolution of rapid evolutionary radiatons requires harvesting maximal signal from phylogenomic datasets. However, studies of non-model clades often target conserved loci that are characterized by reduced information content, which can negatively affect gene tree precision and species tree accuracy. Single nucleotide polymorphism (SNP)-based methods are an underutilized but potentially valuable tool for estimating phylogeny and divergence times because they do not rely on resolved gene trees, allowing information from many or all variant loci to be leveraged in species tree reconstruction. We evaluated the utility of SNP-based methods in resolving phylogeny of Holarctic ground squirrels (Urocitellus), a radiation that has been difficult to disentangle, even in prior phylogenomic studies. We inferred phylogeny from a dataset of >3,000 ultraconserved element loci (UCEs) using two methods (SNAPP, SVDquartets) and compared our results with a new mitogenome phylogeny. We also systematically evaluated how phasing of UCEs improves per-locus information content, inference of topology, and other parameters within each of these SNP-based methods. Phasing improved topological resolution and branch length estimation at shallow levels (within species complexes), but less so at deeper levels, likely reflecting true uncertainty due to ancestral polymorphisms segregating in rapidly diverging lineages. We resolved key clades in Urocitellus and present targeted opportunities for future phylogenomic inquiry. Our results also extend the roadmap for use of SNPs to address vertebrate radiations and inform comparative analyses at multiple temporal scales.

Mammalian body size is determined by interactions between climate, urbanization, and ecological traits.

Anthropogenically-driven climate warming is a hypothesized driver of animal body size reductions. Less understood are effects of other human-caused disturbances on body size, such as urbanization. We compiled 140,499 body size records of over 100 North American mammals to test how climate and human population density, a proxy for urbanization, and their interactions with species traits, impact body size. We tested three hypotheses of body size variation across urbanization gradients: urban heat island effects, habitat fragmentation, and resource availability. Our results demonstrate that both urbanization and temperature influence mammalian body size variation, most often leading to larger individuals, thus supporting the resource availability hypothesis. In addition, life history and other ecological factors play a critical role in mediating the effects of climate and urbanization on body size. Larger mammals and species that utilize thermal buffering are more sensitive to warmer temperatures, while flexibility in activity time appears to be advantageous in urbanized areas. This work highlights the value of using digitized, natural history data to track how human disturbance drives morphological variation.

Digital biodiversity data sets reveal breeding phenology and its drivers in a widespread North American mammal.

Shifts in reproductive timing are among the most commonly documented responses of organisms to global climate change. However, our knowledge of these responses is biased towards taxa that are easily observable and abundant in existing biodiversity data sets. Mammals are common subjects in reproductive biology, but mammalian phenology and its drivers in the wild remain poorly understood because many species are small, secretive, or too labor-intensive to monitor. We took an informatics-based approach to reconstructing breeding phenology in the widespread North American deer mouse (Peromyscus maniculatus) using individual-level reproductive observations from digitized museum specimens and field censuses spanning >100 yr and >45 degrees of latitude. We reconstructed female phenology in different regions and tested the importance of three environmental variables (photoperiod, temperature, precipitation) as breeding cues. Photoperiod and temperature were strong positive and negative breeding cues, respectively, whereas precipitation was not a significant predictor of breeding phenology. However, phenologies and the use of environmental cues varied substantially among regions, and we found evidence that these cueing repertoires are tuned to ecosystem-specific limiting conditions. Our results reiterate the importance of ecological context in optimizing reproduction and demonstrate how harmonization across biodiversity data resources allows new insight into phenology and its drivers in wild mammals.

Body size trends in response to climate and urbanization in the widespread North American deer mouse, Peromyscus maniculatus.

Body size decline is hypothesized to be a key response to climate warming, including warming driven by urban heat islands. However, urbanization may also generate selective gradients for body size increases in smaller endotherms via habitat fragmentation. Here we utilize a densely sampled, multi-source dataset to examine how climate and urbanization affect body size of Peromyscus maniculatus (PEMA), an abundant rodent found across North America. We predicted PEMA would conform to Bergmann's Rule, e.g. larger individuals in colder climates, spatially and temporally. Hypotheses regarding body size in relation to urbanization are less clear; however, with increased food resources due to greater anthropogenic activity, we expected an increase in PEMA size. Spatial mixed-models showed that PEMA conform to Bergmann's Rule and that PEMA were shorter in more urbanized areas. With the inclusion of decade in mixed-models, we found PEMA mass, but not length, is decreasing over time irrespective of climate or population density. We also unexpectedly found that, over time, smaller-bodied populations of PEMA are getting larger, while larger-bodied populations are getting smaller. Our work highlights the importance of using dense spatiotemporal datasets, and modeling frameworks that account for bias, to better disentangle broad-scale climatic and urbanization effects on body size.

Methods for broad-scale plant phenology assessments using citizen scientists' photographs.

PREMISE: Citizen science platforms for sharing photographed digital vouchers, such as iNaturalist, are a promising source of phenology data, but methods and best practices for use have not been developed. Here we introduce methods using Yucca flowering phenology as a case study, because drivers of Yucca phenology are not well understood despite the need to synchronize flowering with obligate pollinators. There is also evidence of recent anomalous winter flowering events, but with unknown spatiotemporal extents. METHODS: We collaboratively developed a rigorous, consensus-based approach for annotating and sharing whole plant and flower presence data from iNaturalist and applied it to Yucca records. We compared spatiotemporal flowering coverage from our annotations with other broad-scale monitoring networks (e.g., the National Phenology Network) in order to determine the unique value of photograph-based citizen science resources. RESULTS: Annotations from iNaturalist were uniquely able to delineate extents of unusual flowering events in Yucca. These events, which occurred in two different regions of the Desert Southwest, did not appear to disrupt the typical-period flowering. DISCUSSION: Our work demonstrates that best practice approaches to scoring iNaturalist records provide fine-scale delimitation of phenological events. This approach can be applied to other plant groups to better understand how phenology responds to changing climate.

A New Species of Sucking Louse from the Long-tailed Ground Squirrel, Urocitellus undulatus, from Mongolia, with a Key to Species, and a Review of Host Associations and Geographical Distributions of Members of the Genus Linognathoides (Psocodea: Anoplura: Polyplacidae).

Members of the genus Linognathoides are ectoparasites of ground squirrels and marmots (Rodentia: Sciuridae) in the Nearctic, Palearctic, and Afrotropical regions. Linognathoides urocitelli n. sp. is described based on adult male and female and third-instar nymphal specimens collected from the long-tailed ground squirrel (Urocitellus undulatus) in Mongolia. The new species is compared morphologically to other members of the genus Linognathoides. Additionally, DNA sequences of a 610-base pair (bp) fragment of the nuclear 18S rDNA gene, a 452-bp fragment of the mitochondrial 12S rrnS gene, and a 363-bp fragment of the mitochondrial 16S rrnL gene are provided. Host associations and geographical distributions of the 11 previously recognized species of the genus, and of Linognathoides urocitelli n. sp., are reviewed. A dichotomous identification key to adults of all known species in the genus Linognathoides is provided.

Impacts of Inference Method and Data set Filtering on Phylogenomic Resolution in a Rapid Radiation of Ground Squirrels (Xerinae: Marmotini).

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.

Mammal collections of the Western Hemisphere: a survey and directory of collections.

As a periodic assessment of the mammal collection resource, the Systematic Collections Committee (SCC) of the American Society of Mammalogists undertakes decadal surveys of the collections held in the Western Hemisphere. The SCC surveyed 429 collections and compiled a directory of 395 active collections containing 5,275,155 catalogued specimens. Over the past decade, 43 collections have been lost or transferred and 38 new or unsurveyed collections were added. Growth in number of total specimens, expansion of genomic resource collections, and substantial gains in digitization and web accessibility were documented, as well as slight shifts in proportional representation of taxonomic groups owing to increasingly balanced geographic representation of collections relative to previous surveys. While we find the overall health of Western Hemisphere collections to be adequate in some areas, gaps in spatial and temporal coverage and clear threats to long-term growth and vitality of these resources have also been identified. Major expansion of the collective mammal collection resource along with a recommitment to appropriate levels of funding will be required to meet the challenges ahead for mammalogists and other users, and to ensure samples are broad and varied enough that unanticipated future needs can be powerfully addressed.

Aproximadamente cada 10 años, el Comité de Colecciones Sistemáticas (CCS) de la Sociedad Americana de Mastozoologia, evalúa el estado de las colecciones mastozoológicas del hemisferio occidental. En el último censo, el CCS encuestó un total de 429 colecciones y compiló un directorio de 395 colecciones activas que contenían 5,275,155 especímenes catalogados. En comparación con el censo previo, durante la última década 43 colecciones se han cerrado o han sido absorbidas, pero se agregaron al censo 38 nuevas colecciones. Se documentó un incremento en el número total de especímenes, la expansión de la disponibilidad de colecciones de recursos genómicos, además de avances substanciales en digitalización y accesibilidad a la web. También, se detectaron cambios en las proporciones de grupos taxonómicos debido a la representación geográfica cada vez más equilibrada de las colecciones en comparación con encuestas anteriores. Si bien consideramos que las colecciones del hemisferio occidental estan en buen estado en algunas áreas, también identificamos brechas claras en la cobertura espacial y temporal, así como amenazas al crecimiento y vitalidad de estos recursos a largo plazo. Un crecimiento substancial, acompañado de compromisos de adecuado financiamiento, serán necesarios para asegurar que las colecciones incluyan muestras lo suficientemente amplias y variadas como para permitir a mastozoologos y otros científicos abordar las necesidades, muchas de ellas imprevistas, que traerá el futuro.

Impacts of late Quaternary environmental change on the long-tailed ground squirrel (Urocitellus undulatus) in Mongolia.

Impacts of Quaternary environmental changes on mammal faunas of central Asia remain poorly understood due to a lack of geographically comprehensive phylogeographic sampling for most species. To help address this knowledge gap, we conducted the most extensive molecular analysis to date of the long-tailed ground squirrel (Urocitellus undulatus Pallas 1778) in Mongolia, a country that comprises the southern core of this species' range. Drawing on material from recent collaborative field expeditions, we genotyped 128 individuals at 2 mitochondrial genes (cytochrome b and cytochrome oxidase I; 1 797 bp total). Phylogenetic inference supports the existence of two deeply divergent infraspecific lineages (corresponding to subspecies U. u. undulatus and U. u. eversmanni), a result in agreement with previous molecular investigations but discordant with patterns of range-wide craniometric and external phenotypic variation. In the widespread westerneversmanni lineage, we recovered geographically-associated clades from the: (a) Khangai, (b) Mongolian Altai, and (c) Govi Altai mountain ranges. Phylogeographic structure in U. u. eversmanni is consistent with an isolation-by-distance model; however, genetic distances are significantly lower than among subspecies, and intra-clade relationships are largely unresolved. The latter patterns, as well as the relatively higher nucleotide polymorphism of populations from the Great Lakes Depression of northwestern Mongolia, suggest a history of range shifts into these lowland areas in response to Pleistocene glaciation and environmental change, followed by upslope movements and mitochondrial lineage sorting with Holocene aridification. Our study illuminates possible historical mechanisms responsible for U. undulatus genetic structure and contributes to a framework for ongoing exploration of mammalian response to past and present climate change in central Asia.

Trait-specific processes of convergence and conservatism shape ecomorphological evolution in ground-dwelling squirrels.

Our understanding of mechanisms operating over deep timescales to shape phenotypic diversity often hinges on linking variation in one or few trait(s) to specific evolutionary processes. When distinct processes are capable of similar phenotypic signatures, however, identifying these drivers is difficult. We explored ecomorphological evolution across a radiation of ground-dwelling squirrels whose history includes convergence and constraint, two processes that can yield similar signatures of standing phenotypic diversity. Using four ecologically relevant trait datasets (body size, cranial, mandibular, and molariform tooth shape), we compared and contrasted variation, covariation, and disparity patterns in a new phylogenetic framework. Strong correlations existed between body size and two skull traits (allometry) and among skull traits themselves (integration). Inferred evolutionary modes were also concordant across traits (Ornstein-Uhlenbeck with two adaptive regimes). However, despite these broad similarities, we found divergent dynamics on the macroevolutionary landscape, with phenotypic disparity being differentially shaped by convergence and conservatism. Such among-trait heterogeneity in process (but not always pattern) reiterates the mosaic nature of morphological evolution, and suggests ground squirrel evolution is poorly captured by single process descriptors. Our results also highlight how use of single traits can bias macroevolutionary inference, affirming the importance of broader trait-bases in understanding phenotypic evolutionary dynamics.

Rapid divergence and gene flow at high latitudes shape the history of Holarctic ground squirrels (Urocitellus).

Across the animal tree of life, the prevalence and evolutionary role(s) of hybridization remain incompletely understood. Rapidly radiating clades can serve as important systems for investigating these issues; however, such groups are often characterized by additional, widespread sources of gene tree discordance (e.g., incomplete lineage sorting). In this paper, we employed a multilocus dataset, Bayesian gene tree inference, and multiple species tree reconstruction methods to infer phylogeny of Holarctic ground squirrels (Urocitellus). We tested phylogenetic hypotheses based on previous morphological, cytological and single-locus datasets, and began to parse the causes of pervasive gene tree discordance that was observed. There is widespread incomplete lineage sorting in Urocitellus, consistent with rapid diversification embedded within the larger radiation of marmotine ground squirrels. We also recovered strong support for 2 instances of mitonuclear discord due to ancient hybridization among members of the high-latitude parryii-richardsonii-elegans clade. These results add to a growing number of documented hybridization events in ground squirrels, suggesting their radiation is a fertile system for understanding the interplay of diversification and hybridization in animal evolution.

Natural history collections-based research: progress, promise, and best practices.

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.

Responses of high-elevation herbaceous plant assemblages to low glacial CO2 concentrations revealed by fossil marmot (Marmota) teeth.

Atmospheric CO2 cycles of the Quaternary likely imposed major constraints on the physiology and growth of C3 plants worldwide. However, the measured record of this remains both geographically and taxonomically sparse. We present the first reconstruction of physiological responses in a late Quaternary high-elevation herbaceous plant community from the Southern Rocky Mountains, USA. We used a novel proxy-fossilized tooth enamel of yellow-bellied marmots (Marmota flaviventris)-which we developed using detailed isotopic analysis of modern individuals. Calculated C isotopic discrimination (Δ) of alpine plants was nearly 2 ‰ lower prior to the Last Glacial Maximum than at present, a response almost identical to that of nonherbaceous taxa from lower elevations. However, initial shifts in Δ aligned most closely with the onset of the late Pleistocene bipolar temperature "seesaw" rather than CO2 increase, indicating unique limitations on glacial-age high-elevation plants may have existed due to both low temperatures and low CO2. Further development of system-specific faunal proxies can help to clarify this and other plant- and ecosystem-level responses to past environmental change.