Putative climate adaptation in American pikas (Ochotona princeps) is associated with copy number variation across environmental gradients.

Improved understanding of the genetic basis of adaptation to climate change is necessary for maintaining global biodiversity moving forward. Studies to date have largely focused on sequence variation, yet there is growing evidence that suggests that changes in genome structure may be an even more significant source of adaptive potential. The American pika (Ochotona princeps) is an alpine specialist that shows some evidence of adaptation to climate along elevational gradients, but previous work has been limited to single nucleotide polymorphism based analyses within a fraction of the species range. Here, we investigated the role of copy number variation underlying patterns of local adaptation in the American pika using genome-wide data previously collected across the entire species range. We identified 37-193 putative copy number variants (CNVs) associated with environmental variation (temperature, precipitation, solar radiation) within each of the six major American pika lineages, with patterns of divergence largely following elevational and latitudinal gradients. Genes associated (n = 158) with independent annotations across lineages, variables, and/or CNVs had functions related to mitochondrial structure/function, immune response, hypoxia, olfaction, and DNA repair. Some of these genes have been previously linked to putative high elevation and/or climate adaptation in other species, suggesting they may serve as important targets in future studies.

Phylogenomics of American pika (Ochotona princeps) lineage diversification.

Quaternary climate oscillations have profoundly influenced current species distributions. For many montane species, these fluctuations were a prominent driver in species range shifts, often resulting in intraspecific diversification, as has been the case for American pikas (Ochotona princeps). Range shifts and population declines in this thermally-sensitive lagomorph have been linked to historical and contemporary environmental changes across its western North American range, with previous research reconstructing five mitochondrial DNA lineages. Here, we paired genome-wide data (25,244 SNPs) with range-wide sampling to re-examine the number and distribution of intra-specific lineages, and investigate patterns of within- and among-lineage divergence and diversity. Our results provide genomic evidence of O. princeps monophyly, reconstructing six distinct lineages that underwent multiple rounds of divergence (0.809-2.81 mya), including a new Central Rocky Mountain lineage. We further found evidence for population differentiation across multiple spatial scales, and reconstructed levels of standing variation comparable to those found in other small mammals. Overall, our findings demonstrate the influence of past glacial cycles on O. princeps lineage diversification, suggest that current subspecific taxonomy may need to be revisited, and provide an important framework for investigations of American pika adaptive potential in the face of anthropogenic climate change.

Late Cenozoic history and the role of Beringia in assembling a Holarctic cestode species complex.

The dynamic climate history that drove sea level fluctuation during past glacial periods mediated the movement of organisms between Asia and North America via the Bering Land Bridge. Investigations of the biogeographic histories of small mammals and their parasites demonstrate facets of a complex history of episodic geographic colonization and refugial isolation that structured diversity across the Holarctic. We use a large multi-locus nuclear DNA sequence dataset to robustly resolve relationships within the cestode genus Arostrilepis (Cyclophyllidea: Hymenolepididae), a widespread parasite of predominantly arvicoline rodents (voles, lemmings). Using this phylogeny, we confirm that several Asian Arostrilepis lineages colonized North America during up to four distinct glacial periods in association with different rodent hosts, consistent with taxon-pulse dynamics. A previously inferred westward dispersal across the land bridge is rejected. We also refine interpretations of past host colonization, providing evidence for several distinct episodes of expanding host range, which probably contributed to diversification by Arostrilepis. Finally, Arostrilepis is shown to be paraphyletic with respect to Hymenandrya thomomyis, a parasite of pocket gophers, confirming that ancient Arostrilepis species colonized new host lineages upon arriving in North America.

Citellinema (Nematoda: Heligmosomidae) from North America with descriptions of 2 new species from the red squirrel Tamiasciurus hudsonicus and 1 from the Canadian woodchuck, Marmota monax.

Citellinema Hall, 1918 includes 6 valid species of gastrointestinal nematodes of sciurids. Two species occur in the Palearctic and 4 in the Nearctic, 3 of which occur minimally across Colorado, Idaho and Oregon and 1, Citellinema bifurcatum, has a wide distribution across North America. Members of the genus are didelphic, possess a cephalic vesicle, a terminal spine-like process in females and feature robust spicules, consisting of a proximal end fused and semicylindrical shaft connected to a lamina supported by 2 terminal filiform processes. Typically, the size of the spicules is used to differentiate species. As part of the Beringian Coevolution Project, specimens provisionally identified as C. bifurcatum were collected through intensive field sampling of mammals and associated parasites from across localities spanning the Holarctic. These specimens revealed considerable genetic variability at both mitochondrial and nuclear loci, supporting the identification of deeply divergent clades. Examination of these new specimens, along with the holotypes of C. bifurcatum and Citellinema quadrivittati indicates that Citellinema monacis (previously synonymized with C. bifurcatum) should be resurrected and 3 additional species described. We suggest that the apparent bifurcated nature of the spicule should be considered a generic diagnostic trait, while the proportional length of the lamina relative to that of the spicule is used as a specific character. We demonstrate the critical need for continued inventory of often poorly known assemblages of hosts and parasites, contributing to a growing baseline of archival specimens, collections and information that make explorations of faunal structure and diversity possible.

Chromosome-Level Reference Genome Assembly for the American Pika (Ochotona princeps).

The American pika (Ochotona princeps) is an alpine lagomorph found throughout western North America. Primarily inhabiting talus slopes at higher elevations (>2000 m), American pikas are well adapted to cold, montane environments. Warming climates on both historical and contemporary scales have contributed to population declines in American pikas, positioning them as a focal mammalian species for investigating the ecological effects of climate change. To support and expand ongoing research efforts, here, we present a highly contiguous and annotated reference genome assembly for the American pika (OchPri4.0). This assembly was produced using Dovetail de novo proximity ligation methods and annotated through the NCBI Eukaryotic Genome Annotation pipeline. The resulting assembly was chromosome- scale, with a total length of 2.23 Gb across 9350 scaffolds and a scaffold N50 of 75.8 Mb. The vast majority (>97%) of the total assembly length was found within 36 large scaffolds; 33 of these scaffolds correlated to whole autosomes, while the X chromosome was covered by 3 large scaffolds. Additionally, we identified 17 enriched gene ontology terms among American pika-specific genes putatively related to adaptation to high-elevation environments. This high-quality genome assembly will serve as a springboard for exploring the evolutionary underpinnings of behavioral, ecological, and taxonomic diversification in pikas as well as broader-scale eco-evolutionary questions pertaining to cold-adapted species in general.

Morphological and molecular characterization of adult hairworms (Phylum Nematomorpha) from Iceland and the Faroe Islands, and documentation of their non-adult stages and hosts.

No species of freshwater Nematomorpha have been described from Iceland, but they have been identified anecdotally. Recent surveys in Iceland using freshwater gastropods as biodiversity indicators resulted in the collection of adult free-living hairworms and their non-adult stages including cysts in snail paratenic hosts and juvenile worms in ground beetle definitive hosts. Additionally, specimens acquired from the Icelandic Institute of Natural History indicate nematomorphs are common in Iceland. A single specimen from the Faroe Islands National Museum represents a new species record. Our morphological and molecular characterization indicated all the samples belong to the species Gordionus wolterstorffii, a common nematomorph found throughout Europe. Also, we provide the first descriptions of the cyst stage for the genus Gordionus. Molecular phylogenetic analysis based on 10 species of Gordionus and one species of the closely related genus Parachordodes indicates that Gordionus is not monophyletic. Combining our morphological and phylogenetic investigations, we discuss the lack of clarity in diagnostic morphological characters and the need for additional global collections to clarify the taxonomy of Gordionus.

When parasites persist: tapeworms survive host extinction and reveal waves of dispersal across Beringia.

Investigations of intercontinental dispersal between Asia and North America reveal complex patterns of geographic expansion, retraction and isolation, yet historical reconstructions are largely limited by the depth of the record that is retained in patterns of extant diversity. Parasites offer a tool for recovering deep historical insights about the biosphere, improving the resolution of past community-level interactions. We explored biogeographic hypotheses regarding the history of dispersal across Beringia, the region intermittently linking Asia and North America, through large-scale multi-locus phylogenetic analyses of the genus Schizorchis, an assemblage of host-specific cestodes in pikas (Lagomorpha: Ochotonidae). Our genetic data support palaeontological evidence for two separate geographic expansions into North America by Ochotona in the late Tertiary, a history that genomic evidence from extant pikas does not record. Pikas descending from the first colonization of Miocene age persisted into the Pliocene, subsequently coming into contact with a second wave of Nearctic colonists from Eurasia before going extinct. Spatial and temporal overlap of historically independent pika populations provided a window for host colonization, allowing persistence of an early parasite lineage in the contemporary fauna following the extinction of its ancestral hosts. Empirical evidence for ancient 'ghost assemblages' of hosts and parasites demonstrates how complex mosaic faunas are assembled in the biosphere through episodes of faunal mixing encompassing parasite lineages across deep and shallow time.

Discovery of Arostrilepis tapeworms (Cyclophyllidea: Hymenolepididae) and new insights for parasite species diversity from Eastern North America.

Species of the genus Arostrilepis were discovered and definitively identified for the first time in rodents from geographically disparate localities along the Appalachian Mountain range of eastern North America (West Virginia, Virginia, and Maine). These are the first confirmed records for species of Arostrilepis occurring east of the Rocky Mountains and the Mississippi River in North America. Arostrilepis gardneri n. sp. is described on the basis of specimens obtained from two phylogenetically divergent rodent hosts: Southern Red-Backed Vole Myodes gapperi (Cricetidae: Arvicolinae) (from West Virginia) and the Woodland Jumping Mouse Napaeozapus insignis (Dipodidae: Zapodinae) (West Virginia, Virginia, and Maine). Additionally, in a mixed infection, specimens of Arostrilepis insperata n. sp. were also found in a Southern Red-Backed Vole from West Virginia. These previously unknown species are primarily distinguished from congeners based on shape, dimensions, and spination (pattern, shape, and size of spines) of the cirrus. Specimens of A. gardneri n. sp. are further characterized by the relative position and length of the cirrus-sac, arrangement of the testes, and relative size of the external seminal vesicle and seminal receptacle. Specimens of A. insperata n. sp. are structurally most similar to A. macrocirrosa from the western Nearctic and Palearctic but with consistently greater dimensions for the cirrus-sac, testes, and seminal receptacle. Phylogenetic analysis of Arostrilepis spp. using partial sequences of the mitochondrial cytochrome b gene and the nuclear second ribosomal internal transcribed spacer strongly supported the status of A. gardneri n. sp. and A. insperata n. sp. within an unresolved clade of congeners in Red-Backed Voles (Myodini and species of Myodes). Our observations extend the known geographic distribution for species of Arostrilepis to the Appalachian Mountains in either a disjunct or possibly continuous but patchy range across North America. Prior observations, summarizing field and museum collections, had suggested that geographic ranges for a diverse assemblage of Arostrilepis in North America were largely restricted to the north-western region of the continent, with historical connections to Beringia and Eurasia. Recognition of a more extensive distribution is consistent with a history of episodic biotic expansion and isolation under a dynamic of taxon pulses for arvicoline rodents and an associated parasite fauna in the Nearctic during the Quaternary. Occurrence in a dipodid rodent represents an event of host colonization from an arvicoline source.

Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites.

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.

Target gene enrichment in the cyclophyllidean cestodes, the most diverse group of tapeworms.

The Cyclophyllidea is the most diverse order of tapeworms, encompassing species that infect all classes of terrestrial tetrapods including humans and domesticated animals. Available phylogenetic reconstructions based either on morphology or molecular data lack the resolution to allow scientists to either propose a solid taxonomy or infer evolutionary associations. Molecular markers available for the Cyclophyllidea mostly include ribosomal DNA and mitochondrial loci. In this study, we identified 3641 single-copy nuclear coding loci by comparing the genomes of Hymenolepis microstoma, Echinococcus granulosus and Taenia solium. We designed RNA baits based on the sequence of H. microstoma, and applied target enrichment and Illumina sequencing to test the utility of those baits to recover loci useful for phylogenetic analyses. We captured DNA from five species of tapeworms representing two families of cyclophyllideans. We obtained an average of 3284 (90%) of the targets from the test samples and then used captured sequences (2 181 361 bp in total; fragment size ranging from 301 to 6969 bp) to reconstruct a phylogeny for the five test species plus the three species for which genomic data are available. The results were consistent with the current consensus regarding cyclophyllidean relationships. To assess the potential for our method to yield informative genetic variation at intraspecific scales, we extracted 14 074 single nucleotide polymorphisms (SNPs) from alignments of four Arostrilepis macrocirrosa and two A. cooki and successfully inferred their relationships. The results showed that our target gene tools yield data sets that provide robust inferences at a range of taxonomic scales in the Cyclophyllidea.

Hymenolepis folkertsi n. sp. (Eucestoda: Hymenolepididae) in the oldfield mouse Peromyscus polionotus (Wagner) (Rodentia: Cricetidae: Neotominae) from the southeastern Nearctic with comments on tapeworm faunal diversity among deer mice.

A previously unrecognized species of hymenolepidid cestode attributable to Hymenolepis is described based on specimens in Peromyscus polionotus, oldfield mouse, from Georgia near the southeastern coast of continental North America. Specimens of Hymenolepis folkertsi n. sp. differ from those attributed to most other species in the genus by having testes arranged in a triangle and a scolex with a prominent rostrum-like protrusion. The newly recognized species is further distinguished by the relative position and length of the cirrus sac, shape of seminal receptacle, and relative size of external seminal vesicle and seminal receptacle. Hymenolepidid cestodes have sporadically been reported among the highly diverse assemblage of Peromyscus which includes 56 distinct species in the Nearctic. Although the host genus has a great temporal duration and is endemic to the Nearctic, current evidence suggests that tapeworm faunal diversity reflects relatively recent assembly through bouts of host switching among other cricetid, murid, and geomyid rodents in sympatry.

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.

Parasite diversity at the Holarctic nexus: species of Arostrilepis (Eucestoda: Hymenolepididae) in voles and lemmings (Cricetidae: Arvicolinae) from greater Beringia.

Previously unrecognized species of hymenolepidid cestodes attributable to Arostrilepis Mas-Coma & Tenora, 1997 in arvicoline rodents from the greater Beringian region and western North America are described. Discovery and characterization of these tapeworms contributes to the recognition of a complex of cryptic species distributed across the Holarctic region. Three species are proposed: Arostrilepis gulyaevi sp. n. is named for cestodes in Myodes rufocanus from the Republic of Buryatia, southeastern Siberia and from the Khabarovskiy Kray, Chukotka Autonomous Okrug, and Magadanskaya Oblast', Russian Far East (western Beringia); A. cooki sp. n. is named for cestodes in Myodes gapperi from British Columbia, Canada and Montana, USA; and A. rauschorum sp. n. is named for cestodes in Microtus oeconomus, M. longicaudus, M. pennsylvanicus and M. xanthognathus from the Brooks Range, Seward Peninsula, north-central interior, and Arctic coastal plains of Alaska (eastern Beringia) and Montana, USA. Consistent with recent studies defining diversity in the genus, the form, size, and spination (pattern, shape and size) of the cirrus are diagnostic; species are further distinguished by the relative position and length of the cirrus sac, and arrangement of the testes. Assessment of genetic data from the cytochrome b gene of mitochondrial DNA complements differentiation of this complex based on morphological attributes and confirms known species diversity within the genus. New data for geographical distribution and host specificity of known Arostrilepis spp. indicate that 3 of 12 recognized species have Holarctic distributions extending across Beringia. These include Arostrilepis beringiensis (Kontrimavichus & Smirnova, 1991) in lemmings (species of Lemmus and Synaptomys), A. cf. janickii Makarikov & Kontrimavichus, 2011 in root voles (M. oeconomus) MAKARIKOV ET AL. 402 · Zootaxa 3608 (6) © 2013 Magnolia Press and A. macrocirrosa Makarikov, Gulyaev & Kontrimavichus, 2011 in red backed voles (species of Myodes) and less often other rodent host species.

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.

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.

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.

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.

Genetic consequences of Pleistocene glaciations for the tundra vole (Microtus oeconomus) in Beringia.

Repeated glacial events during the Pleistocene fragmented and displaced populations throughout the northern continents. Different models of the effects of these climate-driven events predict distinct phylogeographic and population genetic outcomes for high-latitude faunas. The role of glaciations in (i) promoting intraspecific genetic differentiation and (ii) influencing genetic diversity was tested within a phylogeographic framework using the rodent Microtus oeconomus. The spatial focus for the study was Beringia, which spans eastern Siberia and northwestern North America, and was a continental crossroads and potential high arctic refugium during glaciations. Variation in mitochondrial DNA (cytochrome b and control region; 214 individuals) and nuclear DNA (ALDH1 intron; 63 individuals) was investigated across the Beringian region. Close genetic relationships among populations on either side of the Bering Strait are consistent with a history of periodic land connections between North America and Asia. A genetic discontinuity observed in western Beringia between members of a Central Asian clade and a Beringian clade is geographically congruent with glacial advances and with phylogeographic discontinuities identified in other organisms. Divergent island populations in southern Alaska were probably initially isolated by glacial vicariance, but subsequent differentiation has resulted from insularity. Tests of the genetic effects of postglacial colonization were largely consistent with expansion accompanied by founder effect bottlenecking, which yields reduced diversity in populations from recently deglaciated areas. Evidence that populations in the Beringian clade share a history of expansion from a low-diversity ancestral population suggests that Beringia was colonized by a small founder population from central Asia, which subsequently expanded in isolation.