Kayce C. Bell

Divergence with gene flow within the recent chipmunk radiation (Tamias)

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.

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.

Revision of widespread red squirrels (genus: Tamiasciurus) highlights the complexity of speciation within North American forests.

Integration of molecular methods, ecological modeling, and statistical hypothesis testing are increasing our understanding of differentiation within species and phylogenetic relationships among species by revealing environmental connections to evolutionary processes. Within mammals, novel diversity is being discovered and characterized as more complete geographic sampling is coupled with newer multi-disciplinary approaches. North American red squirrels exemplify a forest obligate genus whose species are monitored as indicators of forest ecosystem condition, yet phylogenetic relationships reflecting evolutionary history within this genus remain tentative. Through testing of competing systematic and niche-based divergence hypotheses, we recognize three species, Tamiasciurus douglasii, T. hudsonicus, and T. fremonti. Our data provide evidence of regional differences in evolutionary dynamics and continental gradients of complexity that are important both for future management and for investigating multiple pathways that can lead to the formation of new species.

Phylogenomics from whole genome sequences using aTRAM

&NA; 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.]

Climate change, collections and the classroom: using big data to tackle big problems

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.

Expanded Host Range of Sucking Lice and Pinworms of Western North American Chipmunks

ABSTRACT:  Biological inventories often miss parasites, a critical component of biodiversity, and even well-studied host species generally have a paucity of parasite records. Efforts to document the host diversity and distribution of parasites can use newly collected specimens as well as museum specimens. We focus on a group of widespread, well-documented hosts, western North American chipmunks (Rodentia: genus Tamias). Field-collected and museum specimens of chipmunks from across western North America were examined externally for sucking lice (Anoplura), and gastrointestinal tracts were examined for pinworms (Oxyuriodea). We documented new hosts and expanded the geographic distribution for four parasite taxa under investigation: Hoplopleura arboricola, Neohaematopinus pacificus, Heteroxynema cucullatum, and Rauschtineria eutamii. This effort demonstrates the utility of museum collections as well as the pressing need for continued field collection to characterize global biodiversity.

Sympatric Parasites Have Similar Host-Associated, but Asynchronous, Patterns of Diversification

Parasitism is a common symbiotic interaction across diverse natural systems. Using a comparative evolutionary approach, we investigated the contributions of both host phylogeny and abiotic factors toward diversification of phylogenetically independent endoparasites that inhabit essentially the same physical space. We tested for host-parasite and parasite-parasite phylogenetic concordance in western North American chipmunks (Rodentia: Sciuridae) and two distantly related species of pinworms (Nematoda: Oxyurida). Deep structure in molecular phylogenies revealed signals of host-associated divergence in both parasite species, while shallower phylogeographic structure varied between the two parasites. This suggests that although these parasites experienced similar landscapes and cyclic climate processes, temporally distinctive diversification events were associated with differences in the initiation of their association with host lineages. When climate cycles initiate diversification, partially congruent, but asynchronous, host-associated parasite phylogenies may emerge.

Data from: Impacts of inference method and dataset filtering on phylogenomic resolution in a rapid radiation of ground squirrels (Xerinae: Marmotini)

&NA; 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.

Arctic Museum Collections--Special Issue The Beringian Coevolution Project: Holistic Collections of Mammals and Associated Parasites Reveal Novel Perspectives on Evolutionary and Environmental Change in the North

The Beringian Coevolution Project (BCP), a field program underway in the high northern latitudes since 1999, has focused on building key scientific infrastructure for integrated specimen-based studies on mammals and their associated parasites. BCP has contributed new insights across temporal and spatial scales into how ancient climate and environmental change have shaped faunas, emphasizing processes of assembly, persistence, and diversification across the vast Beringian region. BCP collections also represent baseline records of biotic diversity from across the northern high latitudes at a time of accelerated environmental change. These specimens and associated data form an unmatched resource for identifying hidden diversity, interpreting past responses to climate oscillations, documenting contemporary conditions, and anticipating outcomes for complex biological systems in a regime of ecological perturbation. Because of its dual focus on hosts and parasites, the BCP record also provides a foundation for c...