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Please cite this article in press as: Colella et al., Conservation in a Changing , Trends in Ecology & (2019), https:// doi.org/10.1016/j.tree.2019.09.008

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Review Conservation Genomics in a Changing Arctic

Jocelyn P. Colella,1,5,@,* Sandra L. Talbot,2 Christian Brochmann,3 Eric B. Taylor,4 Eric P. Hoberg,1 and Joseph A. Cook1

Although logistically challenging to study, the Arctic is a bellwether for global change and is Highlights becoming a model for questions pertinent to the persistence of . Disruption of Arctic As a bellwether for global change, ecosystems is accelerating, with impacts ranging from mixing of biotic communities to individual the Arctic is a model for questions behavioral responses. Understanding these changes is crucial for conservation and sustainable pertinent to the persistence and economic development. Genomic approaches are providing transformative insights into biotic management of biodiversity. responses to environmental change, but have seen limited application in the Arctic due to a se- Genomic analyses are transforming ries of limitations. To meet the promise of analyses, we urge rigorous development of our understanding of past Arctic biorepositories from high latitudes to provide essential libraries to improve the conservation, communities, including organismal monitoring, and management of Arctic ecosystems through genomic approaches. responses to historic climate oscil- lations that structured contempo- rary ecosystems. Realizing the Potential of Genomics in the Arctic Arctic warming is occurring two to three times faster than the global mean, causing losses in ice, Accelerating environmental change glacial retreat, and reduced snow cover [1–4]. As environmental change intensifies, the Arctic is now a in the Arctic requires fine-scale focus of geopolitical interest, impacting international commerce, resource extraction, food security, genomic approaches to recognize, document, manage, and monitor the and biodiversity [5,6]. Nevertheless, the Arctic remains one of our most poorly understood biomes pace of biotic disruption. owing to the logistical difficulties and expense of researching this remote [7]. Inextricably tied to Arctic development are shifts in the distributions, interactions, functions, and survivorship Altered species ranges in the Arctic of high-latitude organisms [8,9]. At about 6% of ’s surface, the Arctic provides unparalleled chal- expand opportunities for hybridi- lenges and opportunities to examine community- and ecosystem-level responses to climate disrup- zation, altered selection regimes, tion. Over the past few decades, however, Arctic environmental research has emphasized geophys- range shifts, and the spread of ical processes (e.g., [10]), while our understanding of biotic responses to warming remains pathogens and disease; these and incomplete. other biological attributes can now be revealed with unprecedented power using genomics. Insights into Arctic biodiversity have primarily been derived from paleontology, ecology, , and biogeography at large spatial scales across the Quaternary (e.g., [6,11]). Genomic approaches Geographically broad and tempo- (e.g., [12], see Table 1) are complementary and can access finer-scale processes and patterns. rally deep biorepositories of Arctic Genomics has not been widely applied to polar environments [13], but provides pathways to flora and fauna should be built explore the biotic outcomes of incremental, episodic, or abrupt climate oscillations. In the Arctic, through international collaborations the interplay of incremental warming and extreme events creates considerable exigencies to that leverage existing infrastructure, elucidate and monitor biological responses on regional, landscape, and local scales [14,15]. including field stations, seed banks, and museums, as these specimens Thus, Arctic systems must be on the leading edge of conservation research and management, as will be essential to understanding a foundation for effective anticipation, monitoring, and mitigation of threats posed by emerging and recording changing conditions. pathogens, environmental change, and ultimately leading to elevated rates of [16].

1 Populations accommodate environmental change through migration, phenotypic plasticity, and Department of Biology and Museum of Southwestern Biology, University of New , or they face extirpation. Ecological and evolutionary responses at local and regional Mexico, Albuquerque, NM 87131, USA scales are juxtaposed against efforts to maintain the health and persistence of wild populations 2US Geological Survey, Anchorage, AK despite extreme environmental change. Even short-term responses to change can permanently 99508, USA impact species evolution and persistence. Shifting geographic ranges [17], for example, may trigger 3Natural History Museum, University of secondary contact between previously allopatric populations, prompting hybridization or increasing Oslo, NO-0318 Oslo, Norway 4 competition [18]. Alternatively, range shifts resulting in isolation can impede gene flow and elevate Department of Zoology, Biodiversity Research Centre and Beaty Biodiversity [19]. Such processes have been widely documented using molecular approaches and Museum, University of , often tied to Pleistocene glacial cycles in the Arctic (e.g., [20–23]). Ecological disruption and shifting , BC, ranges also drive new host and parasite associations and disease emergence [24–26]. These scenarios 5http://jpcolella.weebly.com can now be addressed with unprecedented power using next- and third-generation genomic @Twitter: @jociecolella (J.P. Colella). technologies. *Correspondence: [email protected]

Trends in Ecology & Evolution, -- 2019, Vol. --, No. -- https://doi.org/10.1016/j.tree.2019.09.008 1 ª 2019 Elsevier Ltd. All rights reserved. Please cite this article in press as: Colella et al., Conservation Genomics in a Changing Arctic, Trends in Ecology & Evolution (2019), https:// doi.org/10.1016/j.tree.2019.09.008

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Here we discuss ways genomics can be used to understand, mitigate, and monitor unprecedented biotic change in the Arctic and urge better integration of these approaches with existing geophysical Glossary monitoring efforts. Adaptive capacity: the ability to avoid negative impacts of chang- ing environments via plasticity or Learning from Past Episodes of Change microevolutionary change. Although outcomes of Arctic warming vary, the past can be revealed by genomics and contribute to DNA metabarcoding:thesimul- taneous identification of multiple informed forecasts of biotic responses to future change. harbor signatures of deep-time taxa from a single environmental refugial divergence, evolution of genetic incompatibilities, admixture, and genome duplications, sample (e.g., soil, water, scat). while community changes through time can be explored using ancient DNA (aDNA) or environmental Gene drive: the ability of a gene DNA (eDNA). to be inherited more frequently than Mendelian would dictate. The Pleistocene Epoch (2 600 000 to 11 700 years ago) experienced >20 warm–cold climatic cycles, each representing an independent evolutionary experiment of organismal responses to environ- mental oscillations. The formation of vast ice sheets during glaciation exposed continental shelf through lower sea levels (e.g., the Bering Land Bridge), dramatically altering the connectivity and dis- tributions of northern populations. Whole-genome sequencing (WGS) has shed light on demo- graphic impacts of past climate cycles [27]. For example, WGS of Holarctic stoats (ermine; Mustela erminea) revealed signatures of episodic post-glacial expansion and genetic exchange between refugial lineages, coincident with climatic fluctuations [28]. These signatures reflect common demo- graphic trends among Arctic species (Arctic mammals [28], insects [29],plants[20–23], parasites [30], birds [31]), serving as testable models of responses to climate-mediated hybridization. Recurrent signatures of refugial divergence and secondary contact in the genomes of Arctic species underscore the role of environmental change in structuring northern diversity and the power of genomics to elucidate biotic responses.

Advances in sequencing technologies increase the utility of degraded DNA. As the Arctic thaws, well-preserved biological remains released from melting permafrost (e.g., [32]) will shed light on past responses to environmental change. With the Arctic as the ‘last stand’ of northern megafauna, the responses of these now-extinct Arctic species to past change, including fluctuations in , demography, diet, mutualisms, and other factors, can be uncovered with genomic data as we explore intrinsic and extrinsic factors influencing species persistence and evolutionary potential.

Although macrofossils are generally rare and records based on microfossils such as pollen are biased towards certain taxa (e.g., wind-pollinated plants), cold Arctic substrates represent ideal conditions for long-term preservation of time-series DNA deposited by past communities. DNA metabarcoding (see Glossary) [33] has enabled the reconstruction of past Arctic communities from permafrost [34] and lake [35] sediments. Arctic sediments represent a vast but largely untapped archive of change through time. Metabarcoding relies on high-quality reference libraries for taxon identification, typi- cally constructed by sequencing verified specimens in natural history museums (e.g., [36]). Analyses of Arctic permafrost representing the past 50 000 years and diets from the fossilized feces and stomach contents of various megafauna documented a shift from forb-dominated to grass- and shrub-dominated tundra communities perhaps linked to the extinction of northern megafauna [34]. Similar metabarcoding approaches analyzed past communities of fungi [37], extinct megaherbivores such as the woolly rhinoceros [38], and modern Arctic lemming diets [39]. Notably, metabarcoding demonstrated shifts in dominant mutualisms, such as mycorrhiza and N fixation, that are without current analogs [34,40]. While those studies targeted small DNA fragments, future metabarcoding analyses are likely to recover whole genomes from environmental samples, allowing more detailed inference of organismal and community changes.

Recognizing Cryptic Arctic Diversity: A Race Against Time With growing recognition that many Arctic endemics are at increased risk of extinction [41],wemay be in the final age of taxonomic discovery in the north. Proactive systematic inquiry is a critical first step to establish baselines for the measurement, monitoring, and mitigation of change and

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expanded molecular inquiry is expected to uncover substantial cryptic diversity in the Arctic [28,42,43].

The Arctic harbors a spectacular set of archipelagos with geographically restricted endemics vulner- able to warming and other anthropogenic disturbances. Arctic island populations often exhibit lower genetic diversity but greater differentiation from adjacent island populations than nearby continental populations (e.g., [44]). Whether differentiation reflects deeply divergent evolutionary histories or is an artifact of founder effects remains to be tested. Genomics is an invaluable tool for characterizing the standing variation and adaptive potential of insular endemics [43,45].

Arctic remoteness impedes comprehensive assessments of biodiversity, especially in aquatic ecosys- tems. However, data on northern biotic community composition are critical to effective management. Menning et al. [46] developed an eDNA metabarcoding system that simultaneously detects up to 37 Arctic and subarctic freshwater fish species in a single environmental sample. Similarly, eDNA meta- barcoding uncovered multiple pathogens on high-latitude populations of eelgrass by assaying leaves, roots, estuarine sediments, water columns, and migratory bird feces (D. Menning, unpub- lished). Refined eDNA techniques can provide robust, large-scale status assessments of difficult- to-sample high-latitude communities [47], to help monitor changes in biotic composition, species interactions, and life-history events and their consequences for populations [48].

Anticipated Range Shifts: Admixture and Invasions Anticipated northwards invasion by lower-latitude species could lead to competitive displacement or the disruption of predator–prey interactions. Genomics enables the identification of invasion events, source populations, the origins of new environmental interfaces, successful establishment, and sub- sequent patterns of dissemination, all critical to effective responses to emerging infectious diseases (e.g., protostrongylid nematodes in the Canadian Arctic [24,49], anthropogenically driven invasion of vector-borne filarioid nematodes in Fennoscandian ungulates [50]) and other invasives.

Invasions by lower-latitude taxa will increase the frequency of hybridization [18], with profound ecological and economic consequences. Genomic investigations have already demonstrated the ubiquity of historical and contemporary hybridization among high-latitude vertebrates (e.g., birds [51],fishes[52],mammals[28,53]). Accelerated warming may disproportionately favor the replace- ment of cold-adapted species over more gradual in situ adaptation, potentially making adaptive introgression a major factor in the survival and thermal breadth of Arctic species. Genomics serves as a window onto hybridization by quantifying the directionality and strength of introgression, enabling the detection of multiple gene-flow events [28,53] andconnectingtheimpactsofintrogres- sion on fitness [54,55]. Increasing genomic applications in the Arctic is essential to anticipating adaptive lags in species and estimating community resilience. Retrospective evaluation of gene flow associated with historical management initiatives (e.g., assisted gene flow, reintroductions, augmentation [56]) help managers anticipate how natural or human-facilitated hybridization will impact diversity and persistence. Although hybridization was viewed as detrimental to the mainte- nance of biodiversity on shallow timescales, increased genomic resolution has demonstrated that natural hybridization is not only widespread, but may facilitate adaptation to changing climate through the selective incorporation of novel variation [57,58]. For example, introgression from black-tailed jackrabbits (Lepus californicus), which maintain brown winter coats, into winter-white snowshoe hares (Lepus americanus) has enabled the maintenance of brown winter coats in hares at their southern range limits, a key ecological adaptation that may increase hare survivorship in areas with shorter, milder winters and less snow cover [58] (e.g., Figure 1).

Although altitudinal gradients are logistically convenient proxies for understanding terrestrial spe- cies’ responses to warming, the generalization of montane investigations to Arctic systems is limited. Arctic vascular plant genomes document massive range shifts following climatic change that included numerous long-distance dispersal events, often resulting in gene flow between expanding lineages (e.g., [20–23]). Some species recolonized the entire circumpolar area after the last glacial [59] and

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Figure 1. Two Examples of How ‘Omics’ Methods Can Inform the Management and Monitoring of Arctic Flora and Fauna. Symbolic representations of (A) an investigation by Jones et al. [58] that generated whole-genome sequences (WGS) and whole-exome sequences (WES) from winter-white and winter-brown snowshoe hares (Lepus americanus). They discovered that hybridization with black-tailed jackrabbits (L. californicus) at the southern extent of the snowshoe hare range led to adaptive introgression of genes associated with brown coloration, demonstrating that hybridization between Arctic and lower-latitude fauna, as ranges shift, offers a mechanism of adaptation to climate change. (B) Larson et al. [81] used reduced-representation omics methods [restriction- site-associated DNA sequencing (RADseq) and SNP genotyping] to identify and monitor declining Chinook salmon stocks to increase stability of northern fisheries and direct commercial harvests. Plot of the number of Chinook salmon in the Salish Sea 1984–2010 is a symbolic representation of monitoring data from the US Agency [131]. other extreme long-distance dispersal events occurred from the Arctic to [60].Similar patterns were documented in Arctic bryophytes [61], lichens [62], and fungi [63].

Range shifts may also increase isolation. In diploid species, fragmentation reduces the effective pop- ulation size (Ne) and elevates genomic levels of inbreeding, potentially increasing the extinction risk [64]. Although inbreeding is problematic for many vertebrates, widespread selfing in Arctic plants, critical for reliable in the insect-poor Arctic, has led to an autopolyploid majority, with a single individual representing combinations of divergent genomes inherited via hybridization between various diploid progenitor species. Allopolyploidy may mitigate the loss of variation caused by inbreeding and drift [20], a finding with important implications for the conservation of biodiversity. Because a single polyploid plant can carry most of a population’s gene pool, an optimal conservation

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strategy may be to prioritize the persistence of many small populations over fewer large ones [20]. This example emphasizes the importance of considering varied patterns of genome evolution and inheritance in the management of Arctic species.

Thermal fluctuations are rapidly altering physical landscapes in the Arctic, further impacting distribu- tions and connectivity. Reductions in sea ice [65] and permafrost [66] are driving changes in popula- tion structure through dispersal and fragmentation. Landscape genomics facilitates the inference of geographic resistance landscapes based on patterns of gene flow between populations [67], which may be especially informative for exceptionally widespread species like the cyanobacterium Phormidesmis preistleyi, an ecologically important species found at both poles [13].Withasignificant portion of the Arctic’s surface area permanently frozen (<0C), distributions of ice-adapted microor- ganisms [68] are projected to shift significantly. Landscape resistance models can inform pathogen evolution and predict transmission dynamics in natural populations [69].Modelingdemographic and landscape properties from a genomic perspective facilitates the implementation of informed, preemptive management regimes under various warming scenarios to maximize persistence and diversity.

Adaptive Responses to Change In the Arctic, intense environmental selection has led to the repeated evolution of tolerance to freezing and low-light conditions. High-throughput sequencing can enhance the detection of selec- tion and identify genes contributing to local adaptation ([70–72] and N.A.M. Chrismas, PhD thesis, University of Bristol, 2017). Transcriptomic investigations identified post-freezing differential expres- sion profiles that may drive local thermal adaptation (e.g., in earthworms [73],fishes[74],andbarna- cles [75]). With warming temperatures, local cold-adapted taxa may be naturally eliminated. Thus, prioritizing the maintenance of standing , which maximizes the adaptive capacity of species, may prove more effective for the persistence of high-latitude taxa than the conservation of distinct populations.

As a consequence of low temperatures, high moisture, and low nitrogen availability [76],Arcticplants have responded genetically [77] and formed associations with microbial communities (e.g., mycor- rhizal fungi) that can accommodate environmental change [78]. Metagenomics and microbiomics can provide detailed understanding of the molecular mechanisms of nitrogen acquisition in low- temperature environments and the impact of symbiotic relationships on adaptation [78].

Further complicating species survival and management in the Arctic are selective pressures of anthro- pogenic origin. Commercial fisheries, among other resource-extraction pressures, can be selective, aiming to protect individuals with a specific phenotype (e.g., small, female) while optimizing yields [79]. In a few generations, commercial harvests may induce evolution that accelerates life-history changes or alters phenotypes [80]. Loci impacted by fisheries-induced selection can be genomically identified and selected by managers to boost diversity in affected populations and real-time estimates may serve to direct extraction efforts (e.g., Chinook salmon, Oncorhynchus tshawytscha [81]; Figure 1). Changes in genomic architecture, physiology, and functionality have been documented in fishes important to northern subsistence communities (O. tshawytscha [82], Arctoga- dus glacialis [83]), alerting managers to the far-reaching consequences of commercial harvests [84]. Pressure on northern fisheries is expected to increase [85] and a genomic-based management response (Figure 2) could help to maximize resource extraction efficiency while maintaining recover- able population sizes.

Plasticity and Adaptive Capacity Increased variability in weather events (e.g., later spring snowfall) can decouple critical life-history traits such as timing of emergence from hibernation or torpor, breeding, migration, or pollination [86]. As an adaptation to the extreme Arctic environment and seasonal resource limitations, the timing of hibernation is often critical to overwinter survival and shifts have been documented for a number of species. The genomic architecture responsible for inducing and maintaining hibernation

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Figure 2. Effective Implementation of Specimen-Based Conservation Genomics in the Arctic. As recommended by the Arctic Biodiversity Assessment [6], the proposed framework builds collaborative networks (e.g., resource agencies, local communities) of sample collectors to gather critical biomaterials from remote sites (e.g., subsistence hunts) that would then become permanently archived specimens available through natural history collections. Publications communicate critical science to resource managers, planners, and policy makers responsible for conservation and management actions (applied, proactive, and retrospective), while online databases connect diverse investigations and transmit the data, publications, and results to the public. Navy- blue arrows indicate the transfer of specimens and associated data; yellow arrows indicate the flow of information to managers and the public. Colors correspond to Figure 1. Abbreviations: NCBI, National Center for Biotechnology Information; NGO, non-governmental organization. is now being explored [87,88]. Sex-dependent phenological shifts in hibernation [e.g., Arctic ground squirrels (Urocitellus parryii)] [89], due to differing metabolic requirements, or other life-history events may further disrupt reproduction and, ultimately, survival. Premature exposure of young plants to freezing temperatures because of earlier snowmelt has shifted the timing of flowering [90], resulting in lower flower abundance. Large-scale phenological shifts like this can have cascading effects on or- ganisms such as arthropods and herbivores and on soil communities. More detailed documentation

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of genes underlying the timing of life-history events in Arctic species is necessary to understand how rapidly changing environments are impacting biotic systems. Further, understanding the molecular basis of plastic traits can help managers anticipate phenological changes, enabling intentional selec- tion for increased plasticity through captive breeding or source-population selection. Further genomic studies are also needed to characterize the molecular foundation of environmentally induced stress responses in the Arctic [91].

When phenology directly influences individual fitness, it can impact the genetic variability and adap- tive capacity of populations. Climatic warming may trigger earlier migration and breeding (e.g., fishes [92],birds[93,94]), disproportionally impacting species with environmentally constrained or short breeding seasons, common in the Arctic. Shifts in migratory phenology have initiated earlier repro- duction and strong selection against late-migrating pink salmon (Oncorhynchus gorbuscha [92])and similar phenological shifts have been documented for numerous migratory Arctic birds over the past half century. Along the central Arctic coast of Alaska, 16 species now arrive in spring an average of 12 days earlier [93], with differential genomic consequences across species [94]. Research suggests, however, that earlier egg laying in sea-ice-obligate birds (Cepphus grylle mandtii)isbasedon phenotypic plasticity, suggesting that this species may have a limited ability to respond to environ- mental change beyond existing plasticity [95]. Altered phenologies are expected to continue driving mismatches in timing of breeding, migration, and the availability of critical prey species, particularly arthropods, birds, and fish [90]. Investigations into a suite of clock genes involved in circadian or circannual rhythms (reviewed in [96]) have provided preliminary insights into the evolution and regu- lation of these critically linked [97,98]. However, the polygenic nature of environmentally or temporally associated life-history events (see KEGG circadian rhythm pathways [99]) reinforces the importance of a genomic perspective in the examination of these traits.

Emerging Infectious Diseases in the Arctic Parasites have been responsible for substantial mortality in Arctic ungulates [e.g., muskox (Ovibos moschatus), caribou (Rangifer tarandus)], seeding concerns about future subsistence and commercial hunting [100]. Long-term incremental warming and extreme temperature and humidity events drive the colonization of Arctic and subarctic ungulates by vector-borne nematodes [24,49,50].Species- specific genome-wide markers and geographically intensive and site-extensive baselines were instru- mental in the recognition of northwards expansion, host colonization, invasion, and emergence of diseases, which have accelerated recently (e.g., [101]). High-throughput sequencing is especially use- ful for microorganisms, as it requires only trace amounts of DNA but enables the characterization of microbial, parasite, and pathogen distributions and origins, host associations, colonization events, rates, and signal transduction mechanisms controlling behavior, survival, virulence, and gene expression. The discovery of new species and species distributions impacts our understanding of how historical and contemporary forces determine parasite distributions, host ranges, and the po- tential for emerging diseases. The safety and sustainability of traditional foods for northern cultures will benefit from proactive genomic exploration of pathogen prevalence and host–parasite interac- tions across the Arctic [50,102].

The recent discovery of the pathogenic bacterium Erysipelothrix rhusiopathiae associated with widespread mortality in muskoxen from Victoria Island, Canada, is concerning, with over 70% popu- lation loss within a short time [103]. The epidemiology of this pathogen is complex and genomics was central to unraveling its potential origin and dissemination [104,105]. Further, global pathogens are projected to expand on northwards; anthrax emergence recently caused serious mortality in Yamal Peninsula reindeer in Russia [106]. Melting permafrost may release microparasites infecting both humans and wildlife (e.g., [106]). New parasites and pathogens (bacteria, viruses) will continue to emerge [106,107] and expand with declining glacial cover. Genomics is essential to quantifying rates of mutation and monitoring the dispersal of microorganisms and altered host associations. Viruses inhabiting cryoconite holes on glaciers appear to infect a broad range of bacterial species, suggest- ing that warming may have cascading effects on disease dynamics and community composition, as these viruses often control bacterial abundance [108,109].

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Metagenomics can detect invasive parasites, including micro- and macroparasites that encompass diversity ranging from helminths to protozoa, bacteria (pathogenic and commensal), and viruses [110], and provide a critical window onto nutrient and energy cycling and the physiological condition of organisms [57]. Fecal samples can be used to assess starvation stress and identify unhealthy indi- viduals, with direct application to source-population selection for wildlife translocations and disease monitoring. These approaches also permit rigorous exploration of parasite diversity across the land- scape to regional scales (e.g., [111]). Complex microbial community interactions have often been overlooked in management initiatives, despite the importance of various symbioses (e.g., commensal, mutualistic, pathogenic) to survival [112]. Microbial communities, like their hosts, are sen- sitive to external environmental variation and microbial diversity is correlated with habitat quality, which has direct consequences for organismal health and survivorship [113].

Applied Genomics: Intentional and Informed Manipulations The artificial introduction of adaptive , including in genes for increased thermal tolerance, may accelerate adaptive evolution, as is currently being explored in coral symbionts to prevent ther- mally mediated bleaching events [114]. The accelerated rate of Arctic change, combined with limited variation in many high-latitude species, places these taxa on the front lines of experimental applied genomics. Genetic rescue or restoration [115], genomic optimization of captive breeding and in situ recovery programs, de-extinction [116], and offer promising but controversial frontiers for Arctic conservation [117]. The identification of loci involved in [118] can enhance in situ rescue initiatives and ex situ captive-breeding programs. Intentional, informed genetic manipulations have the potential to overcome geographic impediments to gene flow by targeting the negative effects of inbreeding [118] in small populations. Genetic-rescue initia- tives have proved occasionally successful [119] but are not reversible and should be employed judi- ciously due to potential swamping of local variation [115,120].

Gene-drive and genome-editing technologies can perpetuate genetic modifications throughout populations as a potential means of controlling invasive species [121], a major threat facing high-lati- tude species. The efficacy and ethical implications of these new tools have not been fully explored, but such discussions are likely in the next decade. The coupling of gene drive and CRISPR-mediated homology-directed repair mechanisms has facilitated the introgression of antimalarial genes into the Anopheles mosquito vector [122], whose range may expand northwards. for disease control and the integration of artificial resistance may be especially promising for combatting vector- borne diseases (e.g., Jamestown Canyon virus, Snowshoe hare virus, Northway virus – which may also affect humans). Temperature and moisture are instrumental in the development, survival, and trans- mission of many parasites and pathogens; thus, dramatic environmental change in the Arctic is antic- ipated to increasingly alter disease dynamics into the future [24–26].

Concluding Remarks A dearth of accessioned biological specimens – the foundation for monitoring evolutionary response to change – representative of Arctic ecosystems severely limits our ability to successfully apply genomic technologies to high-latitude research and management [7,56]. Due to remoteness and low organismal density [7], northern high-latitude biomes are inherently difficult and expensive to ac- cess, with limited resampling data available from historic sites, both necessary for rigorous assess- ment of change through time.

Quality biological tissues benefit the sequence quality and data volumes generated by high- throughput sequencing methods. Here we urge the development of an internationally coordinated specimen-collection plan [123,124] and propose a framework for the effective implementation of specimen-based conservation genomics in the Arctic (Figure 2) based on recommendations from the Arctic Biodiversity Assessment [6]. Together these initiatives urge the growth of publicly available, specimen-based archives that leverage site-intensive sampling by Arctic rural communities and es- tablished research stations. Collectively, this network will enable the development of taxonomically diverse, geographically broad, and temporally deep (repeated sampling) archives that will capture

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community-level interactions [125–128] (see Outstanding Questions). Such an effort, highlighted in Outstanding Questions the Arctic Biodiversity Assessment [6,14,111], can be accomplished only through broader interna- How best can we build temporally tional collaborations that include multiple stakeholders linking subsistence communities, natural deep and geographically broad resource managers, field stations, natural history collections, genomicists, data scientists, and policy biorepositories for genomic inquiry makers (Figure 2 and Box 1) [127,128]. We identify resource agencies as organizations responsible for into Arctic specimens? How can mandating and permitting the proper archiving of collected biological materials and coordinating these archives be effectively inte- their transport to secure repositories, to ensure the continued utility of these resources for manage- grated into conservation? ment and scientific inquiry, including genomics. Maintenance of biological specimens and access to What are the most powerful the scientific community lies under the purview of natural history collections. Archives should be digi- geographic and taxonomic sam- tally captured and searchable online, so that the specimens and associated data are readily available pling strategies to ensure repre- to diverse research projects for the betterment of science-based assessment, monitoring, and man- sentative sampling of Arctic eco- agement in the rapidly changing Arctic. As use increases with new questions and technological ad- systems? Should we focus efforts vances, the central archiving of natural history specimens and data will facilitate the integration of on abundant taxa, rare taxa, or entire communities? multidisciplinary science (e.g., parasitology, biogeography, systems biology, biomedical sciences) In what ways do biological mate- and expand genomic applications, which we anticipate will be funded by individual research pro- rials (and associated metadata) gramsandorganizations(Figure 2). Genomic information available through peer-reviewed publica- need to be preserved to ensure tions, online data repositories [e.g., National Center for Biotechnology Information (NCBI), Dryad], their usefulness for genomic inquiry and outreach activities can then inform managers and the public to ensure the persistence of healthy and the development of future Arctic communities. technologies? How can we integrate evolutionary Genomic approaches are beginning to reveal unprecedented insights into the mechanisms of local thinking into contemporary man- adaptation, the varied consequences of hybridization, and past responses to climate fluctuations. agement strategies for the effective Fully embracing these new information streams in contemporary conservation and monitoring conservation biological diversity within a timeframe relevant to the rapid environmental change occurring in the Arctic? Given that Arctic ecosystems often Box 1. Calling on Existing Infrastructure host indigenous-majority human The geographically and temporally broad natural history resources necessary to expand genomic applications populations, what approaches are in the Arctic will require a unified network of collaborations among Arctic rural communities, local, regional, necessary such that specimen- and national management agencies, indigenous communities and resource managers, subsistence hunters, based, genomics-focused Arctic trappers, and fishers, field biologists, genomicists, and museum curators (Figure 2). Collaborative sampling biodiversity science can serve as a networks would foster the collection of key samples from remote locations that may prove imperative for doc- model endeavor that truly inte- umenting and understanding biotic responses to accelerating environmental change using genomic ap- grates traditional and technologi- proaches and facilitate the connection of new scientific information (e.g., biotic perturbation, emerging cally focused knowledge systems? pathogens, food insecurity) to process-driven outcomes (e.g., local decision making, public-health response, How does the potential commer- wildlife management) for more efficient and effective stewardship of Arctic resources [132]. Because the Arctic cialization of genomic resources is inherently remote and encompasses multiple countries, samples have been difficult to access, despite the impact biodiversity research at high existence of an international network of biological field stations that could form the backbone of this initiative latitudes? (Figure I). This gap in natural history resources and the current dramatic environmental change characterizing the Arctic [133]] highlights the urgency of collecting and preserving holistic specimens [134] from these re- gions. An international agreement, perhaps through the Arctic Council (https://arctic-council.org), to coordi- nate and fund this effort is needed, but there are numerous established natural history collections with the capacity to receive, store, and distribute these resources, including the University of Alaska Museum of the North, the University of New Mexico’s Museum of Southwestern Biology, the Canadian Museum of Nature in Ottawa, and the University of Oslo’s Natural History Museum in Norway. These act as model cryogenic biorepositories for the expansion of genomic sampling and research in the Arctic.

In addition to capitalizing on existing physical infrastructure (e.g., Arctic field stations, natural history collec- tions), we encourage the parallel expansion of digital biodiversity informatics training and associated resources (e.g., pipelines, data curation). Genomic methods have produced an explosion in data volume, made publicly available through free online resources such as the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA), GenBank, the European Archive (ENA), the European Laboratory (EMBL), the DNA Databank of Japan (DDBJ), and federal data repositories. Equally impor- tant specimen-associated data (and metadata, including physical measurements, GIS collection localities, and morphometric and isotopic data) are, however, notoriously disassociated from other large data streams. Ef- forts to link existing biodiversity informatics databases directly to voucher specimens (e.g., Arctos; https:// arctos.database.museum) will be essential to the integration of scientific disciplines, increased data interoper- ability, and ultimately the conservation of biodiversity in the face of Arctic change.

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Figure I. Arctic Research Stations and Sea Ice Extent (1978 and 2018). Reinvigorated collaborative efforts between Arctic research stations (dots) and natural history museums could provide substantial temporal, spatial, and taxonomic sample coverage to launch genomic inquiry. Current Arctic sea ice extent (August 2018, solid white polygon [134]) and historic sea ice extent (August 1978, white outline), with the Arctic Circle as a thick broken gray line. Abbreviations: ALOMAR, Alomar Observatory; AMUPS, Adam Mickiewicz University Polar Station; CHARS, Canadian High Arctic Research Station; MARS, McGill Arctic Research Station; TERS, Tundra Ecosystem Research Station; Whap.-Kuujj., Whapmagoostui- Kuujjuarapik – Centre d’Etudes Nordiques; WSBS, Biological Station (‘Belomorskaya’).

[129,130] requires the biological sampling infrastructure necessary to produce robust baselines from remote environments (Box 1). This has been largely lacking throughout the Arctic and emphasizes the need to build collaborative, community-based networks there (e.g., [126]) that aim to collect, pre- serve, and provide biological materials necessary to address profound and rapid contemporary change. Observation of biotic change, in the absenceofarchivaldocumentationbasedonspecimens (e.g., physical samples), is insufficient as a pathway to understand and identify broadening and accel- erating trends of ecological disruption at high latitudes.

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