Kurt E. Galbreath

When Cold is Better: Climate-Driven Elevation Shifts Yield Complex Patterns of Diversification and Demography in an Alpine Specialist (American Pika, Ochotona princeps)

The genetic consequences of climate-driven range fluctuation during the Pleistocene have been well studied for temperate species, but cold-adapted (e.g., alpine, arctic) species that may have responded uniquely to past climatic events have received less attention. In particular, we have no a priori expectation for long-term evolutionary consequences of elevation shifts into and out of sky islands by species adapted to alpine habitats. Here, we examined the influence of elevation shifts on genetic differentiation and historical demography in an alpine specialist, the American pika (Ochotona princeps). Pika populations are divided into five genetic lineages that evolved in association with separate mountain systems, rather than lineages that reflect individual sky islands. This suggests a role for glacial-period elevation shifts in promoting gene flow among high-elevation populations and maintaining regional cohesion of genetic lineages. We detected a signature of recent demographic decline in all lineages, consistent with the expectation that Holocene climate warming has driven range retraction in southern lineages, but unexpected for northern populations that presumably represent postglacial expansion. An ecological niche model of past and future pika distributions highlights the influence of climate on species range and indicates that the distribution of genetic diversity may change dramatically with continued climate warming.

Beringia: Intercontinental exchange and diversification of high latitude mammals and their parasites during the Pliocene and Quaternary

ABSTRACT Beringia is the region spanning eastern Asia and northwestern North America that remained ice-free during the full glacial events of the Pleistocene. Numerous questions persist regarding the importance of this region in the evolution of northern faunas. Beringia has been implicated as both a high latitude refugium and as the crossroads (Bering Land Bridge) of the northern continents for boreal mammals. The Beringian Coevolution Project (BCP) is an international collaboration that has provided material to assess the pattern and timing of faunal exchange across the crossroads of the northern continents and the potential impact of past climatic events on differentiation. Mammals and associated parasite specimens have been collected and preserved from more than 200 field sites in eastern Russia, Alaska and northwestern Canada since 1999. Previously, fossils and taxonomic comparisons between Asia and North America mammals have shed light on these events. Molecular phylogenetics based on BCP specimens is now being used to trace the history of faunal exchange and diversification. We have found substantial phylogeographic structure in the Arctic and in Beringia in mustelid carnivores, arvicoline rodents, arctic hares and soricine shrews, including spatially concordant clades and contact zones across taxa that correspond to the edges of Beringia. Among the tapeworms of these mammalian hosts, new perspectives on diversity have also been developed. Arostrilepis horrida (Hymenolepididae) was considered to represent a single widespread and morphologically variable species occurring in a diversity of voles and lemmings in eastern and western Beringia and more broadly across the Holarctic region. The BCP has demonstrated a complex of at least 10 species that are poorly differentiated morphologically. The diversity of Paranoplocephala spp. and Anolocephaloides spp. (Anoplocephalidae) in Beringia included relatively few widespread and morphologically variable species in arvicolines. BCP collections have changed this perspective, allowing the recognition of a series of highly endemic species of Paranoplocephala that demonstrate very narrow host specificity, and additional species complexes among arvicolines. Thus, extensive, previously unrecognized, diversity for tapeworms of 2 major families characterizes the Beringian fauna. By elucidating evolutionary relationships and phylogeographic variation among populations, species and assemblages, refined views of the sequence and timing of biotic expansion, geographic colonization and impact of episodic climate change have been developed for Beringia. Ultimately, Beringia was a determining factor in the structure and biogeography of terrestrial faunas across the Nearctic and Neotropical regions during the Pliocene and Quaternary.

Northern Host–Parasite Assemblages: History and Biogeography on the Borderlands of Episodic Climate and Environmental Transition

Diversity among assemblages of mammalian hosts and parasites in northern terrestrial ecosystems was structured by a deep history of biotic and abiotic change that overlies a complex geographic arena. Since the Pliocene, Holarctic ecosystems assembled in response to shifting climates (glacial and interglacial stages). Cycles of episodic dispersal/isolation and diversification defined northern diversity on landscape to regional scales. Episodes of geographic expansion and colonisation linked Eurasia and North America across Beringia and drove macroevolutionary structure of host and parasite associations. Asynchronous dispersal from centres of origin in Eurasia into the Nearctic resulted in gradients in parasite diversity in the carnivoran, lagomorph, rodent and artiodactyl assemblages we reviewed. Recurrent faunal interchange and isolation in conjunction with episodes of host colonisation have produced a mosaic structure for parasite faunas and considerable cryptic diversity among nematodes and cestodes. Mechanisms of invasion and geographic colonisation leading to the establishment of complex faunal assemblages are equivalent in evolutionary and ecological time, as demonstrated by various explorations of diversity in these high-latitude systems. Our ability to determine historical responses to episodic shifts in global climate may provide a framework for predicting the cascading effects of contemporary environmental change.

Why Museums Matter: A Tale of Pinworms (Oxyuroidea: Heteroxynematidae) Among Pikas (Ochotona princeps and O. collaris) in the American West

Abstract Permanent and well-supported museum or natural history collections provide a solid foundation for the process of systematics research through creation of an empirical record which validates our understanding of the biosphere. We explore the role of museums in ongoing studies of the complex helminth fauna characteristic of pikas (Ochotona spp.) in the American west. These studies address the taxonomy for pinworms of the Labiostomatinae and the problems associated with the absence of adequate type series and vouchers and with misidentifications in original descriptions. We demonstrate that the types for Labiostomum (Labiostomum) coloradensis are identical to some specimens in the syntype series representing L. (Eugenuris) utahensis, although the published descriptions are in disagreement. Both are identical to L. (Eugenuris) talkeetnaeuris and, as a consequence, are reduced as junior synonyms. Only 2 species of large pinworms, namely L. (Labiostomum) rauschi and L. (Eugenuris) talkeetnaeuris, are widely distributed in Ochotona collaris and O. princeps. Although this serves to clarify the taxonomy for species in these genera, prior records remain confused, as representative voucher specimens from all major surveys in North America were never submitted to museum collections. We strongly suggest that type and voucher series should not be held in private or personal collections, where such are eventually lost, discarded, or destroyed through neglect due to inattention and the absence of curation. The potential to accumulate meaningful baselines for assessment of environmental change is jeopardized if materials from survey and inventory are not routinely submitted to museum collections. The capacity of museum repositories, as a focus for systematics, ecology, and evolutionary studies and for the development of resources for biodiversity informatics, continues to be undervalued and poorly utilized by a cadre of scientists who are dependant on accurate and definitive information that transcends specific disciplines.

Finding Them Before They Find Us: Informatics, Parasites, and Environments in Accelerating Climate Change

ABSTRACT: Parasites are agents of disease in humans, livestock, crops, and wildlife and are powerful representations of the ecological and historical context of the diseases they cause. Recognizing a nexus of professional opportunities and global public need, we gathered at the Cedar Point Biological Station of the University of Nebraska in September 2012 to formulate a cooperative and broad platform for providing essential information about the evolution, ecology, and epidemiology of parasites across host groups, parasite groups, geographical regions, and ecosystem types. A general protocol, documentation–assessment–monitoring–action (DAMA), suggests an integrated proposal to build a proactive capacity to understand, anticipate, and respond to the outcomes of accelerating environmental change. We seek to catalyze discussion and mobilize action within the parasitological community and, more widely, among zoologists and disease ecologists at a time of expanding environmental perturbation.

DIVERSITY AND DEMOGRAPHY IN BERINGIA: MULTILOCUS TESTS OF PALEODISTRIBUTION MODELS REVEAL THE COMPLEX HISTORY OF ARCTIC GROUND SQUIRRELS

To assess effects of historical climate change on northern species, we quantified the population history of the arctic ground squirrel (Spermophilus parryii), an arctic‐adapted rodent that evolved in Beringia and was strongly influenced by climatic oscillations of the Quaternary. Competing hypotheses for the species’ population history were derived from patterns of mitochondrial (mtDNA) structure and a bioclimatic envelope model (BEM). Hypotheses invoked (1) sequential isolation of regional populations beginning with the Arctic, (2) deep isolation only across central Alaska, and (3) widespread panmixia, and were tested using coalescent methods applied to eight nuclear (nDNA) loci. The data rejected strict interpretations of all three hypotheses, but perspectives underlying each encompassed aspects of the species’ history. Concordance between mtDNA and nDNA geographic structure revealed three semi‐independently evolving phylogroups, whereas signatures of gene flow at nDNA loci were consistent with a historical contact between certain populations as inferred by the BEM. Demographic growth was inferred for all regions despite expectations of postglacial habitat contraction for parts of Beringia. Our results highlight the complementary perspectives on species’ histories that multiple lines of evidence provide, and underscore the utility of multilocus data for resolving complex population histories relevant to understanding effects of climate change.

Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas

Traditional concepts of the Bering Land Bridge as a zone of predominantly eastward expansion from Eurasia and a staging area for subsequent colonization of lower latitudes in North America led to early inferences regarding biogeographic histories of North American faunas, many of which remain untested. Here we apply a host–parasite comparative phylogeographical (HPCP) approach to evaluate one such history, by testing competing biogeographic hypotheses for five lineages of host-specific parasites shared by the collared pika (Ochotona collaris) and American pika (Ochotona princeps) of North America. We determine whether the southern host species (O. princeps) was descended from a northern ancestor or vice versa. Three parasite phylogenies revealed patterns consistent with the hypothesis of a southern origin, which is corroborated by four additional parasite lineages restricted to O. princeps. This finding reverses the traditional narrative for the origins of North American pikas and highlights the role of dispersal from temperate North America into Beringia in structuring northern diversity considerably prior to the Holocene. By evaluating multiple parasite lineages simultaneously, the study demonstrates the power of HPCP for resolving complex biogeographic histories that are not revealed by characteristics of the host alone.

Resolving the Evolutionary History of Campanula (Campanulaceae) in Western North America

Recent phylogenetic works have begun to address long-standing questions regarding the systematics of Campanula (Campanulaceae). Yet, aspects of the evolutionary history, particularly in northwestern North America, remain unresolved. Thus, our primary goal in this study was to infer the phylogenetic positions of northwestern Campanula species within the greater Campanuloideae tree. We combined new sequence data from 5 markers (atpB, rbcL, matK, and trnL-F regions of the chloroplast and the nuclear ITS) representing 12 species of Campanula with previously published datasets for worldwide campanuloids, allowing us to include approximately 75% of North American Campanuleae in a phylogenetic analysis of the Campanuloideae. Because all but one of North American Campanula species are nested within a single campanuloid subclade (the Rapunculus clade), we conducted a separate set of analyses focused specifically on this group. Our findings show that i) the campanuloids have colonized North America at least 6 times, 4 of which led to radiations, ii) all but one North American campanuloid are nested within the Rapunculus clade, iii) in northwestern North America, a C. piperi – C. lasiocarpa ancestor gave rise to a monophyletic Cordilleran clade that is sister to a clade containing C. rotundifolia, iv) within the Cordilleran clade, C. parryi var. parryi and C. parryi var. idahoensis exhibit a deep, species-level genetic divergence, and v) C. rotundifolia is genetically diverse across its range and polyphyletic. Potential causes of diversification and endemism in northwestern North America are discussed.

Host responses to cycles of climate change shape parasite diversity across North America's Intermountain West

Abstract. Host-parasite cospeciation, in which parasite divergence occurs in response to host divergence, is commonly proposed as a driver of parasite diversification, yet few empirical examples of strict cospeciation exist. Host-parasite co-evolutionary histories commonly reflect complex mosaics of cospeciation, dispersal, lineage extinction and other phenomena. The episodic host-switching model of parasite diversification accounts for complexity by suggesting that diversification and faunal assembly is a consequence of fluctuation between environmental disruption and environmental stability. The phylogeographic predictions of the strict cospeciation and episodic host-switching models were tested using the North American pika/parasite assemblage, with a primary focus on the American pika, Ochotona princeps (Richardson, 1828), and a suite of its endoparasitic cestodes and nematodes. This approach integrating phylogeographic and demographic methods with inferences drawn from species distribution modelling revealed that the parasite community of pikas has been shaped by climate-driven range fluctuation of hosts and bouts of geographic and host colonization by parasites associated with transitions between glacial and interglacial phases.

A widespread distribution for Arostrilepis tenuicirrosa (Eucestoda: Hymenolepididae) in Myodes voles (Cricetidae: Arvicolinae) from the Palearctic based on molecular and morphological evidence: historical and biogeographic implications

Hymenolepidid cestodes in Myodes glareolus from Lithuania and additional specimens originally attributed to Arostrilepis horrida from the Republic of Belarus are now referred to A. tenuicirrosa. Our study includes the first records of A. tenuicirrosa from the European (western) region of the Palearctic, and contributes to the recognition of A. horrida (sensu lato) as a complex of cryptic species distributed broadly across the Holarctic. Specimens of A. tenuicirrosa from Lithuania were compared to cestodes representing apparently disjunct populations in the eastern Palearctic based on structural characters of adult parasites and molecular sequence data from nuclear (ITS2) and mitochondrial (cytochrome b) genes. Morphological and molecular data revealed low levels of divergence between eastern and western populations. Phylogeographic relationships among populations and host biogeographic history suggests that limited intraspecific diversity within A. tenuicirrosa may reflect a Late Pleistocene transcontinental range expansion from an East Asian point of origin.