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 Trends in Ecology & Evolution 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 biodiversity. 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 genome 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 sea 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 region [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 Earth’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, taxonomy, 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 invasive species ultimately leading to elevated rates of extinction [16]. 1 Populations accommodate environmental change through migration, phenotypic plasticity, and Department of Biology and Museum of Southwestern Biology, University of New adaptation, 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 inbreeding [19]. Such processes have been widely documented using molecular approaches and Museum, University of British Columbia, often tied to Pleistocene glacial cycles in the Arctic (e.g., [20–23]). Ecological disruption and shifting Vancouver, BC, Canada 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 Trends in Ecology & Evolution 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. Genomes 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 genetics 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 genetic diversity, 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