Arctic Biodiversity Assessment

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566 Arctic Biodiversity Assessment

The lesser snow goose Chen c. caerulescens shows an approximate east-west cline in their Nearctic breeding distribution in frequency of pale or dark morphs, with blue morphs most common in the east. Although studies of fitness components failed to uncover any adaptive advantage associated with either morph, geese show strong mating preference based on the color of their parents, leading to assortative mating. Queen Maud Gulf Bird Sanctuary, Nunavut, Canada. Photo: Gustaf Samelius. 567

Chapter 17 Genetics

Lead Author Joseph A. Cook

Contributing Authors Christian Brochmann, Sandra L. Talbot, Vadim B. Fedorov, Eric B. Taylor, Risto Väinölä, Eric P. Hoberg, Marina Kholodova, Kristinn P. Magnusson and Tero Mustonen

Contents

Summary ��568 17.5. Recommendations and conservation measures ��582 17.1. Introduction ��568 17.5.1. Call for immediate development of freely available, specimen-based archives ��582 17.2. Systematics, phylogenetics and phylogeography ��569 17.5.1.1. Build European, Asian and North American 17.2.1. Systematics ��569 tissue archives ��582 17.2.1.1. Phylogenetics and taxonomy ��569 17.5.2. Expand biodiversity informatics ��582 17.2.1.2. Systematics and phylogenetics in Arctic species ��569 17.5.2.1. Connect GenBank, EMBL and DDJB to Archives ��582 17.2.2. Phylogeography – setting the stage for interpreting 17.5.2.2. Connect GenBank (Genomics) to GIS applications ��583 changing environmental conditions ��571 17.5.2.3. Stimulate emerging pathogen investigations 17.2.2.1. Influence of dynamic climates on structuring through integrated inventories ��583 Arctic diversity ��571 17.5.2.4. Develop educational interfaces and portals for 17.2.2.2. Contact between divergent populations Arctic databases ��583 or species ��571 17.5.3. Identify, survey and monitor genes that influence fitness ��583 17.2.2.3. Comparisons across species – influence of episodic 17.5.4. Monitor response to climate change (neutral and expansion and isolation on structuring diversity ��572 functional variation) ��583 17.3. Contemporary processes ��577 17.5.5. Management and forensic applications ��584 17.3.1. Demography ��577 17.5.5.1. Ensure rigorous identification ��584 17.3.1.1. Population fluctuation ��577 17.5.5.2. Provide framework for assisted colonization or 17.3.1.2. Effective population size (homozygosity and genetic restoration ��584 heterozygosity) ��577 17.6. Conclusions ��584 17.3.2. Peripheral populations ��577 Acknowledgements ��585 17.3.3. Isolation and endemism ��577 17.3.4. Tracking the invasion of species ��579 References ��585 17.3.5. Identifying emerging pathogens ��580 17.3.6. Threatened and endangered species, ESUs and MUs ��580 17.4. Advances in technology and analytical methods ��580 17.4.1. New technology ��580 17.4.2. New theory and analytical approaches ��581 Knowledge exists, we live it. But I do not think about » that ever. It is just there. We still follow the old ways. Naturally. This is our way. Isak Påve, a Saami reindeer herder from northern Sweden; Hiltunen & Huovari (2004). 568 Arctic Biodiversity Assessment

SUMMARY limited information is available about most essential factors for organisms (e.g. contemporary genetic diversity, The impact of climate warming on Arctic organisms is evolutionary history, modes of reproduction). A coordi- complex, and its interpretation will require a concerted nated investment in biological infrastructure is needed effort. To mitigate the impact of climate-induced per- now (similar to that already in place for monitoring the turbations, an essential first step is to develop an under- physical environment) if we are to apply and realize the standing of how high latitude species and ecosystems powerful insights provided by molecular genetics. were influenced by past episodes of dynamic environmental change. One of our best views of past change in Arctic populations is through molecular genetics (e.g. 17.1. INTRODUCTION DNA studies). DNA-based views provide a basis for fore- casting how biomes and individual species will respond in Maintaining genetic variation in wild populations of Arctic the future and thus are a key component of an advanced organisms is fundamental to the long-term persistence of early-warning system for natural environments of the high latitude biodiversity. Variability is important because Arctic. it provides options for species to respond to changing environmental conditions and novel challenges such as Species typically adapt to new conditions or shift into emerging pathogens or invasive species. As individual spe- new areas, but a number of Arctic species are now ex- cies decline in abundance and their geographic distribu- periencing a reduction in their distributions, abundance tions shrink, genetic variability is also often eroded. It and ability to exchange individuals among populations. is important to realize that we have not yet developed a Molecular genetic approaches are used in a wide range basic understanding of how genetic variability is parti- of studies to provide comprehensive assessments of how tioned across space or time in the Arctic. Furthermore, species interact with their environments. Important in- we lack information on how genetic variation, and the sights have been gained related to the conservation status related concept of evolutionary potential, is generated and of high latitude species of concern, but because Arctic maintained for most Arctic organisms, whether free-living environments are remote and difficult to access, only or parasitic. Fortunately, new technologies and analyti-

Figure 17.1. An Arctic Observatory showing the centrality of a natural history museum to multiple research, teaching, management, policy and outreach initiatives in the Arctic. Of particular importance for molecular genetic analyses is the availability of an archival repository of biotic samples that allow a rapid and rigorous response to emerging natural resource questions. Critical science in several fields related to Arctic biodiversity is now based on molecular genetic approaches and depends on temporally deep and spatially extensive archives for many organisms. Through the development of databases for these archives that are now accessible via the internet, the specimens become central to attempts to connect research to policy and the general public.

Policy initiatives Public Other webtools & databases Universities, Critical science is based (e.g. BOLD, GenBank, GoogleEarth, on molecular genetics Conservation other museums GBIF, Encyclopedia of Life) of Arctic & archives Conservation biology Flora and Fauna • Population status & structure • Abundance • Bottlenecks Sample providers Natural History Museum Long-term Specimen databases (WWW) Ecology environmental • Distribution research stations • Migration Teaching & research, • Dispersal and breeding behavior Pathogen Spatial and temporal perspectives identication & Emerging pathogen detection monitoring • Environmental change • Systematics & population biology • Identication • Monitoring Protected lands • Evolutionary genomics • Health and economic dimensions • Host switching inventory • Range expansion & monitor Evolution Frozen samples of Resource managers • Response to past climate change Arctic fauna & ora • Hybridization Management & research • Historical demography • Parks & protected areas • Forestry services • Fish & wildlife protection

Regional & local commissions • Fish and game managers A molecular approach Specimens & samples Indigenous peoples to Arctic observatories Specimen data and project metadata

Chapter 17 • Genetics 569 cal approaches now afford the possibility of much more covering, categorizing and interpreting biological diversi- comprehensive and refined views of genetic variation, ty. Without this map it is impossible to even ask pertinent but realizing the potential of these new approaches will questions related to change in Arctic environments. Aside foremost require a renewed effort to inventory and rigor- from the more ‘charismatic’ species, our knowledge of ously document Arctic diversity at all levels (Fig. 17.1). the systematics of the vast majority of Arctic organisms A revitalized effort to explore diversity will provide the remains poor. We emphasize two particular aspects of foundation necessary for a variety of theoretical and ap- systematics that are closely interlinked, phylogeny (evo- plied endeavors, ranging from uncovering the history of lutionary relationships) and taxonomy (species delimita- diversification and extinction of organisms, to tracking tion and a standard nomenclature) of Arctic organisms. and mitigating emerging pathogens and invasive species, A strong commitment to these fields is required, if we to developing robust projections for the long-term secu- hope to explore and effectively document diversity and rity of subsistence or traditional foods in the Arctic. ultimately mitigate the impact of environmental change on the outstanding natural environments of the North. Traditional ecological knowledge (TEK) should also be Concurrently, this knowledge contributes to the broader an integral part of Arctic biodiversity assessment (Usher issues of food security as well as sustainability, viability 2000). In particular, this knowledge can help determine and availability of critical biological diversity, which is how to more effectively study Arctic fauna and flora. the cornerstone of subsistence food webs. Systematics For example, rural coastal villages in Alaska have been is, therefore, an integral facet of ecosystem management instrumental in providing unprecedented sampling of ma- and wildlife conservation across the Arctic (e.g. Kutz et rine mammal populations through subsistence harvests. al. 2009a). In Canada, populations of the northern Dolly Varden Salvelinus m. malma are found in the western Arctic region 17.2.1.1. Phylogenetics and taxonomy (i.e. tributaries of the Mackenzie River largely along its western bank), and these are of tremendous significance Phylogenetics is the study of the relationships among vari- to indigenous peoples of the region. The subspecies was ous groups of organisms, based on evolutionary similari- recently assessed as a taxon of Special Concern by Cana- ties and differences. Above the population level, phylo- da’s Committee on the Status of Endangered Wildlife in genetics becomes a history of speciation, with species Canada (COSEWIC 2011). A key feature of the biology viewed as independent lineages (i.e. they are on different of this fish is habitat located within overwintering sites evolutionary trajectories). Phylogenetic trees reveal characterized by groundwater upwelling that maintains history and constrain explanations about the origins and ice-free habitat, and where fish congregate in large num- distribution of biotic diversity. Taxonomy is the theory and bers. Despite the vast extent of occurrence of the subspe- practice of classifying organisms (Mayr 1969). Early taxo- cies’ distribution across the western sub-Arctic (e.g. ~ nomic studies relied almost exclusively on morphological 227,000 km2), these essential overwintering sites number variation, but now new ways of probing diversity based fewer than 20 and have a combined area of less than 1 on molecular genetics are providing more refined views km2. The locations and the limited numbers of these key of geographic variation. Limitations imposed by a poorly habitats were obtained in large part from TEK which was, developed taxonomic framework can have disastrous con- therefore, critical to the status assessment and subsequent servation consequences (Mace 2004). Taxonomy provides derivation of a conservation management plan. the classification system for organisms that is the basis for rigorous project design and efficient prioritization of This chapter does not tackle the thorny issues related to funding. More than just providing a universally accepted bio-prospecting and commercialization of Arctic genomic name or common language for scientists and managers, resources or introduction of genetically modified organ- though, a taxonomic framework should accurately reflect isms. Instead, we provide an overview of not-for-profit the evolutionary relationships among organisms. System- approaches to studying genetic diversity in the Arctic atics and taxonomy places history on the table and pro- emphasizing that an understanding of the influence of vides the direct connections linking evolution, ecology deeper (evolutionary) time in structuring diversity is and biogeography. This predictive framework then allows essential to predicting future responses and persistence us to rapidly investigate and identify emerging threats of the incomparable fauna and flora of the northern high such as the presence of pathogens and disease (Vapalahti latitudes of our planet. et al. 1999, Brooks & Hoberg 2006, Dragoo et al. 2006, Kang et al. 2009).

17.2. SYSTEMATICS, PHYLOGENETICS 17.2.1.2. Systematics and phylogenetics in Arctic AND PHYLOGEOGRAPHY species In general, incomplete taxonomic information and dis- 17.2.1. Systematics crepancies in identification between studies have severely hampered efforts to quantify the number of extant More than any other approach, systematics integrates species globally and to delineate their respective ranges. across all other sub-disciplines of the biological sciences The Arctic is no exception. There are large gaps in our by establishing the evolutionary map necessary for dis- knowledge of Arctic biodiversity for certain groups, such 570 Arctic Biodiversity Assessment as the marine, terrestrial and freshwater invertebrates nome doubling), which in most studied cases originated (Hardy et al. 2011, Hodkinson, Chapter 7). However, after hybridization between divergent lineages. Recent, even for better-studied groups of Arctic organisms, such recurrent polyploid evolution in plants, associated with as vertebrates and vascular plants (Appendix 17.1), the climate shifts and postglacial colonization (reviewed in ability to identify important forces shaping biodiversity is Brochmann et al. 2004) appears to be positively corre- complicated. Vascular plants exemplify this complexity. lated with latitude. As much as 73% of Arctic specialists are polyploids; more than half of these are hexaploids or Next to vertebrates, vascular plants represent the most- higher. Although there is no clear-cut association between explored group of Arctic organisms in terms of systemat- the frequency or level of polyploidy and degree of glacia- ics. Progress towards a unified Arctic-wide taxonomy for tion, for Arctic specialists with restricted distributions, vascular plants has long been hampered by widely different the frequency of diploids is much higher in unglaciated traditions among European, Russian and North American Beringia than in the heavily glaciated Atlantic area. This plant taxonomists (see Daniëls et al., Chapter 9). Inherent suggests that polyploids are more successful at colonizing problems in the Arctic flora persist, including notorious after deglaciation. Polyploidy results in highly heterozy- taxonomic complexities due to hybridization, reticulate gous genomes buffering against inbreeding depression evolution, inbreeding/asexuality and occurrence of very and loss of genetic variability following long-distant widespread species with complex morphological variation. colonization and through periods of climate change. A Nevertheless, recent progress has been made in the pro- polyploid combines and preserves, in modified form, the duction of the first consensus checklist for all Arctic vas- genomes of all of the original diploid progenitor species. cular plant species (VPAF-The PanArctic Flora Checklist; The average ploidy level of the 1,000 taxa in the regular Elven 2011), in which many plant groups are revised based Arctic flora is pentaploid. These Arctic plant species thus on recent molecular studies. Approximately 2,200 species represent many more species (perhaps some 2,500) in and subspecies are listed in VPAF, but only about 1,000 of terms of genetic or ‘ancestral species’ diversity. Also, them are part of the regular Arctic flora; the remainder are there is a link between polyploidy and genetic diversity in mainly boreal taxa that only have occasional Arctic occur- Cladocera (Hodkinson, Chapter 7). rences. Only 106 taxa can be classified as Arctic endemics, i.e. with their ranges limited to the Arctic (Daniëls et al., There is abundant molecular evidence for recurrent for- Chapter 9). mation of Arctic polyploids from more or less divergent diploid or low-polyploid progenitors, and this may be an The Arctic flora, considered young in evolutionary important means of incorporating several alleles at each terms, is inferred to have formed only 2-3 million years locus. The high frequency of self-pollinating and asexual ago when continuous Tertiary forests gave way to the reproductive systems (Brochmann & Steen 1999), and tundra ecosystem in response to a colder climate. The reshuffling of populations during the glacial cycles has flora is composed of a mixture of lineages resulting from resulted in taxonomically intricate and high-polyploid immigration from southern mountains, dispersal across species complexes in many plant groups. New genetic and Beringia, in situ Pleistocene speciation and probably analytical approaches can disentangle ancestral sub-genom- in situ survival of some Tertiary forest elements (Mur- es, making it possible to demonstrate recent and dynamic ray 1995, Ickert-Bond et al. 2009). Evidence suggests evolution of Arctic polyploid species complexes (Brysting that some Arctic plant species, such as mountain sorrel et al. 2007; Appendix 17.1). These approaches can also be Oxyria digyna and Iceland purslane Koenigia islandica are used to identify cryptic variation in Arctic species. probably very old (Murray 1995), while others, such as purple saxifrage Saxifraga oppositifolia, netleaf wil- Identifying cryptic variation low Salix reticulata, black crowberry Empetrum nigrum, Research on cryptic species has increased over the past bog blueberry Vaccinium uliginosum, Arctic white heather two decades, largely fueled by increasing availability Cassiope tetragona and mountain avens Dryas octopetala, of molecular data, including large-scale campaigns to are thought to have colonized the Arctic approximately generate and catalog DNA sequence data (DNA ‘bar- 3 million years ago, most often from Beringia (Bennike coding’) that have revealed divergent groups not previ- & Böcher 1990, Matthews & Ovenden 1990, Abbott et ously detected using morphological analyses (Appendix al. 2000). Molecular data for several other Arctic plant 17.2). Biological species diversity in the Arctic may be groups show major episodes of speciation that occurred higher than the number of currently recognized species. recently, probably within the period of the major ice ages While biodiversity in the Arctic is likely underestimated (< 1million years; Brochmann et al. 2003, 2004, Broch- in poorly-known species (Hardy et al. 2011), previously mann & Brysting 2008). Phylogenetic reconstruction and unidentified genetic diversity has been uncovered there DNA barcoding (Hebert et al. 2004) in many Arctic plant in invertebrates that had been assessed with traditional groups demonstrate little within-genus variation or none morphological approaches (Hodkinson, Chapter 7) and at all (Appendix 17.1), suggestive of recent speciation in even in the most well-studied taxonomic groups, such spite of conspicuous morphological divergence (Carlsen as vertebrates and plants (Appendix 17.2). For example, 2007, Sønstebø et al. 2010). the depth of mtDNA phylogenetic splits in two genera of Arctic lemmings suggests that continuous vicariant sepa- Pleistocene speciation in Arctic plant groups occurred ration by glacial barriers over several glacial-interglacial both at the diploid level and via polyploidization (ge- cycles resulted in cryptic speciation across the Holarctic Chapter 17 • Genetics 571

(lemmings: Lemmus; Fedorov et al. 1999a, 2003, Dicros- of geographic colonization, host switching and varying tonyx; Fedorov & Goropashnaya 1999). Coincidentally, degrees of cospeciation that provide substantial insights substantial cryptic diversity has been demonstrated for conservation in the Arctic (e.g. Hoberg & Brooks for parasites circulating among assemblages of Arctic 2008, 2010, Koehler et al. 2009). mammals (e.g. Cook et al. 2005). For avian species, DNA barcodes have uncovered Arctic species with deep 17.2.2. Phylogeography – setting the intraspecific divergence (Kerr et al. 2007) that is thought to result from vicariant separation over several glacial stage for interpreting changing cycles (Appendix 17.2). For Arctic plants, selfing pro- environmental conditions vides instantaneous isolation from other lineages, thereby Assessment of the spatial distribution of genealogical facilitating the accumulation of hybrid incompatibilities. lineages within species is called phylogeography (Avise For example, in Arctic withlow grasses Draba spp., rapid 2000, Knowles 2009, Hickerson et al. 2010), a relatively development of sterility barriers resulted in numer- new field that bridges phylogenetic (macroevolution) and ous but cryptic biological species within single diploid population genetic (microevolution) analyses. Phyloge- taxonomic species, to an extent unknown in other floras ography enables us to develop fundamental insights about or plant groups (Brochmann et al. 1993, Grundt et al. evolutionary origins, biogeographic barriers, refugia, his- 2006). Their recent Pleistocene origin suggests that cryp- torical demography, concordant genetic patterns of dif- tic speciation was rapid and possibly facilitated by genetic ferent species within a single ecosystem, temporal niche drift (Grundt et al. 2004, 2006, Skrede et al. 2008). conservatism, and evolutionarily significant units (ESUs). Ultimately, these biotic and abiotic attributes allow a Coevolution of parasites and hosts: range of future responses of species to be predicted. Examples from mammals More than 40-50% of the organisms on the planet are 17.2.2.1. Influence of dynamic climates on structuring parasites. Terrestrial, aquatic and marine systems all Arctic diversity support diverse faunas of worms, arthropods, protozo- ans, bacteria and viruses dependant on vertebrate and The contemporary distribution of genetic diversity in invertebrate hosts. Parasites are not passive players, and Arctic organisms points to potential areas of long-term interactions among parasites and their hosts shape eco- persistence of populations, possible directions of coloni- systems and food webs (Hudson et al. 2006, Dobson et zation, and areas where distinct biotic communities may al. 2008, Hoberg & Kutz, Chapter 15). Elegant research come into contact and exchange pathogens (e.g. Koehler in parasitology has been conducted at high latitudes, et al. 2009). The Arctic is an exceptional system for ex- particularly studies focusing on parasites transmissible amining the influence of climatic events on the patterns to people (termed zoonoses) (e.g. Rausch 1951, 1967, and processes of genetic differentiation and prospects 2003), but in many ways we still are only beginning to for long-term persistence among diverse organisms. A explore the extremely diverse world of these organisms. fundamental question is whether different species are New studies emphasize the power of integrated survey responding to climate change in much the same way, or is and inventory involving geographically extensive and site each species independent (i.e. are there idiosyncratic sig- intensive field collections in conjunction with molecu- nals across multiple species)? Furthermore, how do their lar approaches to understanding diversity in complex responses influence population structure and life history? biological systems in the North. Across the Arctic, for How does this view of history then feed into predictions example, arvicoline rodents (e.g. Microtus, Myodes, Lem- about dynamic change in these systems? mus, Synaptomys and Dicrostonyx) share long coevolutionary histories with two groups of parasitic tapeworms: the 17.2.2.2. Contact between divergent populations or anoplocephalines, Anoplocephaloides spp. & Paranoplo- species cephala spp., and hymenolepidids Arostrilepis spp. (Rausch 1952, Haukisalmi et al. 2006, 2008, Haukisalmi 2009, Locales where different species or distinctive popula- Hoberg et al. 2012a). Both the host and parasite faunas tions come together or contact each other are of special appear to harbor substantial cryptic diversity that is just interest to biologists and can be studied using molecular now being revealed through application of genetic tools genetic techniques (Hewitt 2011). If multiple species to a large series of newly available samples from across show similar patterns of contact, then these sites may the Arctic (e.g. Haukisalmi et al. 2001, 2002, 2004, 2008, represent suture zones (Remington 1968) and may be Hoberg et al. 2003, Wickström et al. 2003, 2005, Cook especially important to conserve. Are contact zones et al. 2005). Similar cryptic lineages have been observed spatially and temporally contemporaneous across species? among nematodes in free-ranging ungulates, pointing Although warming environmental conditions should be toward considerably broader host and geographic ranges detrimental for many Arctic species, others may expe- for pathogenic parasites in caribou (named reindeer in rience increased genetic variability, if contact occurs Eurasia) Rangifer tarandus, moose Alces americanus, wild between previously separate populations or species (Box sheep Ovis spp. and muskoxen Ovibos moschatus (e.g. 17.1). When divergent Arctic populations of the same Jenkins et al. 2005, Kutz et al. 2007, Hoberg et al. 2008) species or of closely related species contact and inter- than previously described. Comparisons of host and breed, the contact may lead to hybrid vigor and increased parasite DNA-based phylogenies reveal complex histories evolutionary potential, allowing organisms to cope with 572 Arctic Biodiversity Assessment

Box 17.1. Contemporary contact zones Box 17.2. Historic contact zones

A zone of secondary contact between two divergent Fish may experience the most extensive losses of genetic groups of Lemmus lemmings likely reflecting recurrent variability among vertebrate species. For example, two isolation by the North American ice sheets was recently species of char (genus Salvelinus) come into contact in the detected in central-eastern Alaska and Yukon (Fedorov Arctic basins of eastern Asia and western North America. et al. 2003). Phylogenetic division between these two Dolly Varden S. malma are distributed in the western and groups was consistently supported by sequence variation eastern portions of the Arctic in the Pacific Basin. Arc- in three independent genetic markers: mtDNA, X and Y tic char S. alpinus exhibit a wider, Holarctic distribution chromosome introns (Fedorov & Goropashnaya 2009). throughout northern Europe, Asia and North America (see Variation in these markers across the secondary contact Fig. 6.3 in Christiansen & Reist, Chapter 6). The two species zone revealed a limited number of introgressants (17%) are broadly sympatric at least in the western Arctic basin of largely one hybrid type, suggesting that reproductive of North America. Genetic and morphological analysis isolation in these lemmings may be the result of separa- of contact zones in two lakes in western Alaska suggest tion by continental ice sheets during Pleistocene glacial the two species exhibit strong habitat partitioning in advances. This newly characterized contact zone contains sympatry (Dolly Varden in streams, small ponds and rivers; the highest genetic diversity in these lemmings, and is Arctic char in larger lakes), and show little evidence of situated in protected national parks (Wrangell-St. Elias, contemporary hybridization. Mitochondrial DNA analysis, Yukon-Charley and Gates of the Arctic). This lemming hy- however, suggested that the species have undergone brid zone provides an impetus for similar analyses in other hybridization historically, presumably under different species from this region, with implications for multi-spe- environmental conditions, suggesting that changing cies or community-level conservation strategies to ensure climates may impact their level of genetic and ecological the maintenance of high levels of genetic variability. interaction (Taylor et al. 2008).

altered environments. In some situations, contact may Holocene transition (Sokolov & Zhirnov 1998). Some be detrimental by causing the disruption of coadapted herbivore species, such as caribou, retained their circum- gene complexes, extinction by hybridization (Rhymer & polar range, while others experienced dramatic range Simberloff 1996, Taylor et al. 2006), opportunities for contraction (Box 17.3 and 17.4). Such shifting patterns of host-switching by pathogens, or possible rearrangement sympatry and abundance have been considered as primary of pathogen genomes that increases virulence. Instances drivers for parasite faunal structure among Holarctic of past contact can be uncovered with molecular genetics ungulates (e.g. Hoberg 2005, 2010). Investigations of the (Box 17.2). phylogeography of these species, especially those comparative studies that include both modern and ancient DNA, are helping to establish the reasons for widespread 17.2.2.3. Comparisons across species – influence extirpation or extinction of elements of the megafauna, of episodic expansion and isolation on and can also provide insight into more contemporary pat- structuring diversity terns associated with domestication (Box 17.3). Repeated changes in climate during the Pleistocene caused Arctic species to move, adapt or go extinct. During We gain insight into how species in the Arctic will the late Pleistocene, the Arctic megafauna experienced respond to future conditions by examining how they significant changes in geographic distribution and com- responded to past environmental changes. Molecular position. Some Arctic large herbivores, such as mammoth markers, along with fossils, provide that window into the Mammuthus primigenius and woolly rhinoceros Coelodonta past (e.g. Dalen et al. 2007). For species that moved, re- antiquitatis became extinct, while others, such as saiga peated contractions and expansions influenced evolution- antelope Saiga tatarica, caribou and muskox survived ary processes and left genetic signatures (Hewitt 2004, into the present, but not necessarily at high latitudes Excoffier et al. 2009) within species now inhabiting the (Appendix 17.3, Box 17.3 and 17.4). The causes of the Arctic. Species were fragmented into localized popula- late Pleistocene megafaunal extinctions are not totally tions by glacial advances (e.g. many terrestrial species) understood, but changes in the climate, the arrival of or contractions (e.g. marine species) during the Ice Ages. humans, or a combination of these events may have served Some of the cold-adapted Arctic species persisted during as triggers (Barnosky et al. 2004, Guthrie 2006). The warm interglacials in northern refugia, expanding their survival strategy of large herbivores was different. For ranges southward during glacial periods (e.g. Markova example, the nearly circumpolar Pleistocene distribution et al. 1995). Some cold-adapted species persisted to the of the nomadic saiga antelope shifted to the dry steppe south of continental ice sheets (lemmings, pikas Ochotona and semi-desert regions of Europe and Central Asia after spp.) and then shifted northward (Fedorov & Goro- the tundra-steppe ecosystems were replaced by taiga pashnaya 1999, Fedorov et al. 2003, Lessa et al. 2003). forests after climate amelioration during the Pleistocene- In some cases, species persisted in multiple refugia and Chapter 17 • Genetics 573

Box 17.3. Genes reflect the history of domestication

Phylogeography provides the evolutionary framework for coexisting widely across the region (Baskin 2000, Reimers studying the history of domestication in caribou that al- & Colman 2006, Reid et al., Chapter 3). About 50% of the lows us to identify the number of reindeer domestication approximate 3 million Eurasian reindeer are wild, and events. Phylogeographic relationships within caribou/ many of their herds coexist with domestic reindeer in the reindeer reflect historical patterns of fragmentation and same areas (Baskin 2005). Analyses of DNA markers have colonization rather than clear-cut relationships among revealed at least three independent origins of domestic extant populations and subspecies. Analyses of mitochon- reindeer in Eurasia. drial DNA has revealed that the three subspecies of small- bodied, high Arctic caribou had multiple, independent Genetic differences among reindeer show that the Saami origins (Flagstad & Røed 2003). The three major genetic people of Fennoscandia domesticated their own reindeer groups presumably represented three separate popula- independently of the indigenous cultures in western Rus- tions during the last glacial: the largest of these popula- sia. Augmentation of domestic reindeer herds by crossing tions represented an extensive and continuous glacial with wild animals has been common in most parts of the population across Beringia and far into Eurasia; a smaller, range, but absent in some localities. These data do not more localized population was isolated and restricted to a support the single origin hypothesis that posited that refugium resulting from ice expansion in western Eurasia; domestic reindeer first appeared a few thousand years and several discrete populations were distributed in ago east of the Urals in the southern part of the Siberian glacial refugia presumably located south of the ice sheet taiga and then spread to other regions (Røed et al. 2008). in North America (Flagstad & Røed 2003). Such a finding has immediate implications for the genetic management of these herds, especially in terms of ge- In Eurasia, domestication of the reindeer is considered to netic restoration efforts (Hedrick 2005). be in the early phases, with wild and domestic herds still

Box 17.4. Genes reflect changes in distribution and abundance

Unlike caribou, the muskox was relatively abundant Remarkable distribution and abundance changes have during the Pleistocene, but endemic populations are also been demonstrated in the saiga antelope. Prior now restricted to Greenland, the central Canadian Arctic to the Holocene, the range of this mammal spanned and the Arctic archipelago; re-introduced populations from France to the Northwest Territories of Canada, but are present in Alaska, Canada, Russia and Fennoscandia. subsequently contracted to the steppes of SE Europe Analyses of mtDNA variation reveal that muskox genetic and Central Asia, where historical records indicate that it diversity was much higher during the Pleistocene than at remained extremely abundant until the end of the Soviet present (MacPhee et al. 2005, Campos et al. 2010a, 2010b). Union. After that, its populations were reduced by over Campos and coauthors have shown that there were multi- 95%. Phylogenetic analyses of mtDNA of ancient and ple expansions and contractions of the species range over modern saiga specimens revealed the existence of two the past 60,000 years. Their genetic analyses demonstrate well-supported, and clearly distinct, clades of saiga. The that population dynamics of muskox are better explained first, spanning a time range from > 49,500 14C YBP to the by nonanthropogenic causes, a hypothesis supported by present, comprises all the modern specimens and ancient historic observations on the sensitivity of the species to samples from the northern Urals, middle Urals and NE both climatic warming and fluctuations. In northeastern Yakutia. The second clade is exclusive to the northern Siberia, which held a large diverse population until local Urals and includes samples dating from between 40,400 extinction at ≈ 45,000 radiocarbon years before present to 10,250 14C YBP. Current genetic diversity is much lower (14C YBP), genetic diversity and presumably population than that present during the Pleistocene. The observed size increased about 30,000 14C YBP, contracted about data are more compatible with a drastic population size 18,000 14C YBP, and finally recovered in the middle reduction (c. 66-77%) following either a demographic bot- Holocene. The arrival of humans into relevant areas of tleneck in the course of the Holocene or late Pleistocene, the muskox range did not affect levels of mitochondrial or geographic fragmentation (followed by local extinc- diversity (Campos et al. 2010a). It is thought that reduced tion of one subpopulation) at the Pleistocene/Holocene genetic diversity in muskoxen may render these ungu- transition (Campos et al. 2010b). lates particularly sensitive to exotic parasites and pathogens (e.g. Kutz et al. 2004). 574 Arctic Biodiversity Assessment then expanded from multiple sources (collared lemming 2002, Brunhoff et al. 2003, Galbreath & Cook 2004). Dicrostonyx torquatus; Fedorov & Stenseth 2002, common Genetic studies of Arctic species showing overall high lev- eider Somateria mollissima; Sonsthagen et al. 2011). Multi- els of genetic diversity have verified the role of Beringia cellular organisms also survived glacial periods in refugia as a major refugium (Hultén 1937, Abbott & Brochmann beneath ice sheets as reported for two endemic ground- 2003). In addition, these studies led to the discovery of water crustaceans, Crangonyx islandicus and Crymostygius additional northern refugia (Fedorov & Stenseth 2001, thingvallensis, recently discovered in Iceland (Kornobis 2002, Worley et al. 2004, Waltari & Cook 2005, Loehr et et al. 2010). Identifying this complex history of expan- al. 2006) that are further supported by paleoecology (e.g. sion and contraction lays a foundation for predicting how Kullman 2008) and ecological niche modeling (Hope et species will respond in the future and thus for focusing al. 2010, Galbreath et al. 2011). Cold- and ice-adapted conservation efforts. Arctic species should see more fragmentation and greatly reduced ranges as climate warms. Thus, genetic diversity Terrestrial taxa of cold-adapted Arctic species may have been influenced The phylogeographic history of some Arctic terrestrial by warm climatic events during interglacials and the species and species complexes are now known in some Holocene differently from temperate taxa (Box 17.5). detail (Appendix 17.3). Some terrestrial species, such as hemispherical draba Draba subcapitata, alpine rockcress During glacial maxima, many species apparently occu- Arabis alpina, glacier buttercup Ranunculus glacialis, king pied southern refugia (Stewart et al. 2010), recolonizing eider Somateria spectabilis, Arctic fox Vulpes lagopus, polar northward following the retreat of the Fennoscandian bear Ursus maritimus and snowy owl Bubo scandiacus (Paet- ice sheet in Europe (Hewitt 1996, 2001, Schmitt 2007) kau et al. 1999, Schönswetter et al. 2003, Pearce et al. and the Laurentide and Cordilleran ice sheets in North 2004, Dalen et al. 2005, Ehrich et al. 2008, Marthinsen et America (Runck & Cook 2005, Weckworth et al. 2010). al. 2009, Skrede et al. 2009) show little genetic diversity Much of eastern Europe, Siberia and North America, and/or structuring across the Arctic (Appendix 17.3), however, remained virtually ice-free. Beringia was a large due in part perhaps to repeated bottlenecks during refugium during glacial advances, and multiple plant postglacial colonization coupled with low philopatry and species recolonized the Arctic from refugia after the ice high levels of dispersal. However, many terrestrial species sheets receded (Hultén 1937). Due to isolation from show some degree of genetic structuring (e.g. Cladocera, other populations, different refugia typically harbor di- carabid beetles, butterflies; Hodkinson, Chapter 7) with vergent lineages of species, suggesting that ice age refugia identifiable populations or distinct genetic groups. Some promoted diversification at high latitudes (Fedorov et al. plants harbor considerable genetic diversity in addition 2003). to that associated with polyploidy. Large-scale phylogeographic patterns exist in the Arctic (Eidesen 2007, In addition to its role as a cradle that generated new Waltari et al. 2007), and it is clear that Pleistocene glacia- species, Beringia and the Bering Land Bridge acted as a tions had a major impact on overall genetic diversity and crossroads between Eurasia and North America during its distribution over Arctic landscapes. For many species, glacial periods allowing for the transcontinental migra- gene flow in the Arctic is severely hampered by long- tion of plants and animals (e.g. Waltari et al. 2007). The standing physical barriers, including the Atlantic Ocean, influence of the Bering Strait often is not reflected in the Bering Strait, the Greenlandic Ice Cap, the Ural and genetic analyses of terrestrial organisms suggesting that Mackenzie Mountains, and the lowlands between Euro- this oceanic divide between Asia and North America pean Arctic and southern alpine areas. For Arctic plants, (most recently formed 11,000 years ago) has minimally high mobility appears to be a clue to understanding influenced divergence within Holarctic mammals (Brun- diversification within species and as a driver of specia- hoff et al. 2003, Galbreath & Cook 2004) and some birds, tion. In Arctic plants, long-distance colonization occurs including migratory species (Pearce et al. 2004, 2005, at a much higher rate than previously thought. Although Reeves et al. 2008). In a number of avian species (Zink physical barriers such as oceans have hampered gene flow et al. 1995, Wenink et al. 1996) and terrestrial mammals in the Arctic relative to continuous land-masses, recent that are ecologically associated with dry environments, cross-oceanic dispersal has occurred in many species however, this barrier delineates significant genetic breaks (Alsos et al. 2007), including mountain avens and bog (Fedorov & Goropashnaya 1999, Fedorov et al. 1999b, blueberry. Wickström et al. 2003). Some species that share habitats and distributions show idiosyncratic histories with regard The boundaries of evolutionary groups within many to expansion out of high latitude refugia, and thus are different terrestrial Arctic species are concentrated near sensitive to different barriers (Box 17.6). Similarly, the mountain ranges that were formerly glaciated. For exam- Bering Land Bridge acted as a dispersal filter for trans- ple, birds (e.g. dunlin Caladris alpina) and rodents (Lem- continental migration of some plant taxa, while other mus, Dicrostonyx, Microtus oeconomus) share suture zones plant species never crossed the Bering Strait (DeChaine where distinct evolutionary groups come together, and 2009, Ickert-Bond et al. 2009). these correlate to the western (Kolyma Mountain up- lands) and the eastern (Mackenzie River/eastern Alaska Range shifts following climate change in some species Range) borders of Beringia (Hewitt 1996, Wenink et al. have not, however, followed the classical temperate mod- 1996, Fedorov et al. 1999b, 2003, Fedorov & Stenseth el of genetic depauperation through repeated bottlenecks Chapter 17 • Genetics 575

restricted to refugia under the current climate (nodding saxifrage Saxifraga cernua, mountain avens, bog blueberry; Box 17.5. Cold-adapted species Appendix 17.3). These species apparently proliferated in respond differently than vast tundra populations during most of the Pleistocene warm-adapted with high genetic diversity found not only in areas little affected by the major Pleistocene ice sheets, such as Ber- Arctic-adapted collared lemmings demonstrate low ingia, but also in areas that were colonized postglacially genetic diversity in northern regions affected by north- by several distinct lineages (mountain avens; Appendix ward forest expansions in the Eurasian Arctic during 17.3). In some cases (e.g. purple saxifrage; Abbott et al. the Holocene climate warming. The low genetic diver- 2000, Abbott & Brochmann 2003), genetic data support sity and timing of population expansion suggest that Hultén’s (1937) suggestion that Arctic plants radiated populations of the collared lemming went through east- and westward from Beringia and reached a full reduction in effective population size due to range circumpolar distribution prior to the onset of the Pleis- contraction during warming events (Fedorov 1999). tocene glaciations. During Pleistocene glaciation cycles, This hypothesis that cold adapted species will see a the circumpolar range repeatedly fragmented into (and reduction in population sizes was recently supported then was recolonized from) several refugia. However, using ancient DNA analyses when a drastic reduction the genetic patterns differ for other Arctic plant species. in effective population size during Late Pleistocene and For example, Arctic white heather Cassiope tetragona ssp. Holocene warming events was demonstrated in one tetragona (Eidesen et al. 2007) demonstrates low genetic population of the collared lemming in the northern Pre diversity consistent with a much more recent history of Urals (Prost et al. 2010). Beringian origin, westward expansion one glacial cycle ago, and eastward expansion possibly as recent as the Holocene. Similar multiple expansions out of Berin- gia are demonstrated in cloudberry Rubus chamaemorus (Ehrich et al. 2008) and alpine brook saxifrage Saxifraga Box 17.6. Barriers to transcontinental rivularis (Westergaard et al. 2010), although details vary. movement Truly Arctic marine and freshwater taxa Two high latitude trans-Beringian migratory passer- Relatively little is known about the levels of genetic ines, the Arctic warbler Phylloscopus borealis and the diversity in truly Arctic marine organisms, except for eastern yellow wagtail Motacilla tschutschensis are a few mammal (e.g. walrus Odobenus rosmarus, beluga both asymmetrically distributed across Beringia, with Delphinapterus leucas, bowhead Balaena mysticetus) and fish extensive range in the Palearctic, and a limited occur- species. For those taxa that do not depend on the coastal rence in the Nearctic. Both species occupy mixed habi- zone, the Arctic represents a relatively continuous envi- tats along streams and rivers, and birds in breeding ronment where no essential subdivision is expected, and populations of both species in eastern Beringia winter a uniform gene pool should be the rule, but this pattern in the Palearctic. Phylogeographic studies (Reeves has been observed even for coastal Arctic species (e.g. the 2008, Reeves et al. 2008) show that both species are opossum shrimps Mysis oculata, M. nordenskioldi, M. seger- characterized by shallowly-diverged clades that sorted stralei; Audzijonyte & Väinölä 2006, 2007). Such homoge- geographically. The Beringian clade of the Arctic neity contrasts with clearer subdivision in similar amphi- warbler is found in both eastern and western Beringia, Atlantic comparisons of boreal taxa that retain signatures and the clade does not overlap with Palearctic clades. of distinctive stocks (i.e. trans-oceanic endemism) that Conversely, the Beringian eastern yellow wagtail clade survived on opposite trans-oceanic coasts (e.g. Wares & shows stronger affinity to eastern Beringia, while the Cunningham 2001). In some species, the role and effects Alaskan and Asian clades overlap geographically. of post-glacial dispersal from refugia across the current Reeves (2008) found that the Arctic warbler displayed Arctic is reflected in decreasing genetic variation as dis- a divergence zone at the Lena-Kolyma barrier, but the tance from putative refugial areas increases, most notably barrier for the eastern yellow wagtail correlated with Beringia (cladoceran crustaceans [Weider & Hobæk the Bering Strait. Furthermore, the wagtail colonized 2003], freshwater and anadromous salmonid fish [Stam- eastern Beringia earlier than the Arctic warbler. ford & Taylor 2004, Harris & Taylor 2010]). The effects of Arctic climate on intraspecific genetic structure are also observed in the predominance of shifts from sexual to clonal modes of reproduction (apomixis or automixis), during colonization (Hewitt 1996). Many cold-adapted such as in freshwater Cladocera (Hebert et al. 2007). Arctic plant species may have shifted their large distributions in response to glacial cycles (Hewitt & Nichols The Arctic Basin as a migration corridor and contact area 2005). Many of these species were probably more widely of Atlantic-Pacific marine lineages distributed during cold periods, rather than restricted to For the principally Arctic marine taxa, the Arctic Basin smaller refugia (e.g. dwarf willow Salix herbacea; Appen- may represent a single pool. Many other marine species dix 17.3). In some Arctic plants, northern populations are mainly sub-Arctic and often extend to the boreal are more variable than southern ones, where they are zone. This overall distribution is often discontinuous, 576 Arctic Biodiversity Assessment with broad gaps in the central Siberian and Canadian during glaciations, and subsequent dispersal to the Arctic coastal and archipelago sectors, and between disjunct basin with ameliorating climates followed by secondary sub-ranges on the Atlantic and Pacific (Bering Sea) contact and then occasionally mixing of genomes (Ap- fringes. These discontinuities reflect the post-glacial pendix 17.3). Particularly, in M. balthica such contact expansion from Pacific and Atlantic ‘refugial’ sources along the Arctic margins of the Barents and White Seas, and indicate that trans-Arctic connections existed during as well as the Baltic, have led to amalgamation of di- climatically favorable periods. Genetic structure is often verged genomic origins into widespread hybrid swarms. reflected in a trans-Arctic vicariance of Atlantic and These can be seen as newly evolved taxa with extraordi- Pacific sister taxa or lineages. Molecular data indicate nary levels of genetic diversity that entered new habitat significant variation across taxa in this amphi-boreal/ in the Arctic-boreal marginal seas during the Holocene amphi-sub-Arctic relationship and in structuring Arctic (Strelkov et al. 2007, Nikula et al. 2008). In the future, genetic diversity. For a number of species, exemplified by the frequency of dissolved isolation barriers and genesis the sea urchins Strongylocentrotus spp., patterns of hap- of qualitatively new diversity should increase as a con- lotype sharing between Atlantic and Pacific populations sequence of the changing climate and human-assisted indicate effectively continuous exchange across the Arctic trans-Arctic dispersal. Such contacts of Atlantic (boreal) (Palumbi & Kessling 1991, Addison & Hart 2005). For and trans-Arctic (Pacific origin) lineages in the northeast- others, the presence of distinct lineages points to effec- ern European sub-Arctic are known from morphologi- tive isolation for 3 million years, since the fundamental cal evidence for a number of fish taxa (i.e. the Pechora/ cooling of the climate and origin of the Arctic environ- White Sea populations of Atlantic/Pacific herring, Clupea ment. This longer isolation is reflected in the morphology harengus, C. pallasii and smelt; Osmerus eperlanus, O. dentex; of some taxa, but remains cryptic in others (e.g. Ortí et Berger 2001). Such trans-Arctic vicariant events also ap- al. 1994, Taylor & Dodson 1994, Nikula et al. 2007). In ply to within-basin distributions (McAllister 1963, Ilves some taxa, vicariance across the Arctic has probably been & Taylor 2009), with the potential for similar losses of important in driving subsequent speciation within the isolating barriers among more recently diverged lineages Atlantic and Pacific sub-Arctic basins. For example, these and at smaller spatial scales. patterns have been explored in complex assemblages of tapeworm parasites among seabirds and marine mam- Arctic marine – freshwater vicariance (‘glacial relicts’) mals, although these systems have yet to be explored A number of fish, seal and crustacean taxa typical of Arc- based on phylogeographic approaches (Hoberg 1992, tic estuaries occupy vicariant ranges in the cold waters Hoberg & Adams 2000). Additionally, the rockfish genus of deep boreal lakes, the Baltic Sea and even the Caspian Sebastes, for instance, consists of a species flock of about Sea and Lake Baikal, and are known as ‘glacial relicts’ 110 species in the North Pacific and only four species in or the ‘Arctic element’. Their genealogical relationships the North Atlantic (Love et al. 2002). The latter probably (who descended from whom, and when) are a subject of stem from speciation following trans-Arctic dispersal long-lasting speculation (e.g. Segerstråle 1976). Genetic from the North Pacific (Johns & Avise 1998). data contributes to our understanding of these relationships, indicating long-standing independence of the main It is also clear that alternating episodes of isolation and boreal populations (i.e. Caspian and Baikal inland taxa connection between freshwater habitats across marine in Asia and inland taxa in North America) from Arctic barriers (e.g. repeated opening and closing of the Bering populations (Väinölä et al. 2001, Audzijonyte & Väinölä Land Bridge/Strait) has been important in structur- 2005, Audzijonyte et al. 2005, Palo & Väinölä 2006). In ing species dispersal and phylogeographic patterns. The contrast, lake populations on northern coasts do not dif- Arctic grayling Thymallus arcticus probably originated in fer from adjacent Arctic estuarine lineages (e.g. shrimp the eastern Siberia (Froufe et al. 2003, Weiss et al. 2006). Gammaracanthus and opossum shrimps Mysis; Väinölä et Both the European T. thymallus and the Arctic grayling al. 2001, Audzijonyte & Väinölä 2006). Still, in several dispersed widely to the west from this presumed area of cases there is a close relationship of particular boreal lake origin, and the Arctic grayling also dispersed east into populations to the Arctic main range, indicating recent Arctic regions of North America as far as Hudson Bay ‘relict’ status for these lake populations (Ferguson et al. (Stamford & Taylor 2004). Such dispersal in a primary 1978, Audzijonyte & Väinölä 2006). In still other cases, freshwater fish must have taken place in freshwaters such as sculpins within the genus Myoxcephalus, the depth of the Bering Land Bridge (the Arctic grayling is also and inferred time of divergence of freshwater popula- present on St. Lawrence Island within the Bering Sea). tions from the ancestral Arctic fourhorn sculpin M. Interestingly, mtDNA and microsatellite DNA evidence quadricornis appears to differ between North American suggest that some secondary dispersal of Arctic grayling deepwater sculpins M. (q.) thompsonii and European fresh- back into Siberia has occurred historically (Stamford & water populations of fourhorn sculpin M. q. quadricornis Taylor 2004). (Kontula & Väinölä 2003). Likewise, the ice-breeding ringed seals Pusa hispida of the Baltic Sea and Fennoscan- In the Arctic, genetic structure of marine species, exem- dian lakes are true post-glacial ’Arctic relicts’ isolated plified by capelin Mallotus villosus (Dodson et al. 2007) from the main stock that now occupies the Arctic in large and bivalves (Macoma balthica and Mytilus spp.; Nikula numbers. Some of these marginal populations show signs et al. 2007, Rawson & Harper 2009) often reflects both of extreme depletion of genetic variation in post-glacial deep subdivision traceable to inter-oceanic isolation time (Palo et al. 2001, 2003). Chapter 17 • Genetics 577

17.3. CONTEMPORARY PROCESSES alone is not necessarily predictive of population decline due to inbreeding. Many Arctic plants are regularly and predominantly self-pollinating, leading to very small ef- 17.3.1. Demography fective population sizes and, in diploid species, high levels of homozygosity. Because the majority of truly Arctic 17.3.1.1. Population fluctuation plants are polyploids and combine divergent genomes inherited from various diploid progenitor species, they It is axiomatic in conservation biology that the ability of a can retain extremely high levels of heterozygosity in spite population to respond to current ecological and evo- of inbreeding (‘fixed heterozygosity’). For example, a lutionary forces is partially dependent upon the main- 16-ploid selfing plant, the cushioned draba Draba cor- tenance of genetic diversity. Populations that undergo ymbosa, combines the genomes of eight original diploid large reductions in the number of effective breeders are progenitor species, with a single plant theoretically expected to exhibit reduced levels of genetic variation. harboring 16 different alleles per locus. Six alleles have Extinction risk increases in small, isolated populations been identified at one locus to date (Brochmann & Steen due to negative effects associated with genetic drift, such 1999, Brochmann et al. 2004). Polyploidy in Arctic plants as the erosion of quantitative genetic variation required may serve as an escape from losses of genetic and eco- for adaptive evolution (Westemeier et al. 1998, England logical variation caused by inbreeding and genetic drift et al. 2003) and inbreeding depression (Mills & Smouse (Brochmann & Elven 1992), a finding with important 1994, Saccheri et al. 1998). These expectations have been consequences for conservation. Because a single plant can corroborated empirically. Spielman et al. (2004) report carry most of a population’s gene pool (in the form of that 74% of threatened avian species demonstrate lower fixed heterozygosity), the optimal conservation strategy levels of heterozygosity than non-threatened sister taxa, for many Arctic plants is to conserve many small popula- and that threatened populations demonstrate a 35% re- tions rather than a few large populations (Brochmann & duction in heterozygosity vs. non-threatened populations Steen 1999). (see Frankham et al. 2002 for review). Prior knowledge that a population has endured a recent, severe popula- 17.3.2. Peripheral populations tion decline can help managers anticipate problems, such as decreased reproductive fitness, reduced survival and Although peripheral populations may have reduced levels increased susceptibility to disease, even though cur- of variability, these populations often harbor unique al- rent population size may not suggest risks. Because past leles that comprise a significant portion of the genetic fluctuations in population numbers are often undetect- variability maintained by individual species. Hence, able, genetic data can help to infer how both recent and peripheral or isolated populations become key factors in historical demographic, ecological and genetic histories the long-term persistence of individual species. Novel of species interact to affect persistence. Such assess- genetic variability in peripheral populations may increase ments are crucial to management prescriptions applied the adaptive potential necessary for species to respond to recovering populations of endangered species (Brown- to novel challenges (Box 17.7). At the northern distri- Gladden et al. 1997), such as the widely distributed but butional margins, conserving evolutionary processes in likely never abundant peregrine falcon Falco peregrinus peripheral populations on the edge of species distribu- (Johnson et al. 2010). Some populations of this species tion may be important to northward range shifts (Lessica recently recovered from severe declines in the Arctic and & Allendorf 1995, Hampe & Petit 2005, Gibson et al. elsewhere during the last half of the 20th century, due to 2009). The circumpolar plant, drooping saxifrage, con- effects associated with the bioaccumulation of chlorin- tains genetically variable Arctic populations (Gabrielsen ated hydrocarbons. & Brochmann 1998, Kjølner et al. 2006) and isolated, genetically depauperate populations in southern mountains (e.g. the Alps). However, southern peripheral popula- 17.3.1.2. Effective population size (homozygosity and tions in the Ural Mountains were genetically enriched via heterozygosity) hybridization with a diploid ancestor, bract saxifrage S. Populations of Arctic organisms, especially those in iso- sibirica (Kapralov et al. 2006). lated populations at the southern periphery of distributions and those in the high Arctic, could become reduced 17.3.3. Isolation and endemism in size or further isolated as a result of climate warming. Smaller populations may experience higher inbreeding, The Arctic includes a spectacular set of islands and increasing the possibility that highly deleterious reces- archipelagos that support a number of species, some of sive alleles are expressed (Hedrick & Kalinowski 2000). which are restricted (endemic) to particular islands. Island Isolation has profound effects on genetic variability and endemics are particularly vulnerable to climate warming ultimately on the ability of a species to withstand envi- and other anthropogenic disturbances such as the intro- ronmental or biotic challenges. Wright’s (1931, 1938) duction of invasive alien species (Vitousek et al. 1995), but effective population size (Ne) is a fundamental parameter our understanding of most Arctic archipelagos is limited in many population models that can be used to monitor (Box 17.8 and 17.9). If specimens are available, molecu- populations that have experienced decreases (Johnson lar genetic analyses allow us to readily identify endemic et al. 2010). However, low effective population size organisms and monitor changes to insular faunas and 578 Arctic Biodiversity Assessment

Box 17.7. Peripheral populations can evolve rapidly

Rapid evolution can occur when a peripheral population tochondrial data from the fossil polar bear demonstrated becomes isolated with no gene flow and evolves rapidly that polar bears survived the last interglacial warming to a novel adaptive optimum, as hypothesized for polar period of ~ 130,000-110,000 years ago, and suggested bears and brown bears Ursus arctos and corroborated by that modern polar bear populations experienced a recent fossil and genetic evidence. Studies of fossils indicated and rapid expansion throughout the Arctic since the Late polar bears diverged from the more widely distributed Pleistocene, perhaps followed by a climate-related popu- brown bear. Kurtén (1964) suggested polar bears became lation bottleneck. isolated on Siberian coastal enclaves during the mid-to- late Pleistocene (100,000-70,000 years ago) and became In contrast, comparative analyses of nuclear genomes increasingly specialized as carnivores hunting solely on of the same and additional brown and polar bears, and sea ice. Genetic studies confirm the close relationship an American black bear, placed the divergence of polar between brown and polar bear, and further demonstrate and brown bear at approximately 4-5 million years ago, that brown bears occupying Admiralty, Chichagof and coinciding with the Miocene-Pliocene boundary, a period Baranof (ABC) islands of southeast Alaska’s Alexander of environmental change that may have launched a Archipelago share a mitochondrial DNA lineage more radiation of bear species (Krause et al. 2008). Subsequent closely related polar bears than to other brown bears (Tal- to this ancient split, the two species embarked on largely bot & Shields 1996). This mtDNA lineage may have been independent evolutionary trajectories. In addition to the more widely distributed, possibly becoming isolated on mitochondrial genome, however, 5-10% of the nuclear refugia during the Wisconsinan glaciation, and remaining genome of the enigmatic ABC brown bears is ‘polar restricted recently. bear-like’, suggesting the initial split was apparently followed by occasional admixture that left a clear polar bear Lindqvist et al. (2010) and Miller et al. (2012) conducted imprint on the nuclear genomes of the ABC bears. Further, ancient DNA analyses on the lower jawbone of a polar the nuclear genome-based analyses uncovered historical bear excavated in-situ at Poolepynten, on Svalbard. Long- fluctuations in effective population size (the number of term stratigraphic studies of the Poolepynten site, includ- breeding bear individuals, Ne) that strongly indicate polar ing dating of both sediments and the jawbone, suggested bear evolution tracked key climatic events since the Late the ancient polar bear lived between 110,000 to 130,000 Pleistocene. While considerably larger in the past, polar years ago, the oldest polar bear fossil known. Using high- bear Ne declined during periods of long-term climate throughput ‘next-generation’ sequencing technology, change. Lower genetic diversity observed in extant polar these researchers generated a complete, multifold-cover- bears relative to brown bears is consistent with a pro- age of the mitochondrial genome (Lindqvist et al. 2010), longed and considerable population bottleneck in polar followed by shallow genomic sequencing (Miller et al., bear, coupled with recent expansions from small founder 2012) of this specimen, to compare to deeply sequenced populations, as estimated from the mitogenomic data. mitochondrial and nuclear genomes of extant polar and brown bears. Analyses included the enigmatic ABC brown Despite ancient admixture and population fluctuations, bears that are characterized by mitochondrial DNA se- the unique evolutionary pathway taken by polar bears quences as more similar to those of polar bears than other since their divergence from brown bears is reflected in brown bears (Talbot & Shields 1996). unique genomic signatures. Miller et al. (2012) identified potential regions of genes in polar bears that may relate Comparative analyses of mitochondrial DNA genomes to adaptation to the Arctic environment, including placed the ancient polar bear almost directly at the genes controlling fatty acid metabolism, hibernation, branching point between polar bears and the ABC brown and pigmentation. Such studies in paleobiology have bear lineage, consistent with the divergence of polar dramatic implications for conservation biology includ- bears from within brown bears approximately 150,000 ing predicting responses to anthropogenic climate years ago, or with an ancient hybridization event. The mi- change (Dietl & Flessa 2011).

floras which typically are highly susceptible to extinction tion that caused a significant difference in fitness (relative (Diamond 1989, Olson 1989, Burkey 1995, Blackburn et survival rate) between cod adapted to shallow water and al. 2004, Whittaker & Fernandez-Palacios 2007). those adapted to deep water. The length and age at which the fish matured also decreased. These findings provide Molecular population genetics can also demonstrate general lessons for population and conservation genetics, other forms of cryptic isolation among populations. A showing that anthropogenic changes in habitat can lead molecular study detected that the marine Atlantic cod to intense selection even if the mortality is non-selective Gadus morhua were subjected to fisheries-induced evolu- in the habitat in which it occurs. The study highlights the Chapter 17 • Genetics 579

Box 17.8. Distinguishing endemics Box 17.9 Insular populations from exotics can be heavily impacted

Cook et al. (2010) analyzed variation in mitochondrial The concept of island endemics also applies to species sequences and nuclear microsatellite loci across more on mountaintops (‘sky islands’) and aquatic organisms than 200 Arctic ground squirrels Spermophilus parryii in lakes. For instance, semi-isolated populations of representing 17 populations in western Alaska (12 on Atlantic cod Gadus morhua occur in three saline lakes islands of the North Pacific). Significant geographic on islands in the Canadian Arctic Archipelago (Hardie structure suggests a combination of both long-term et al. 2006). These populations show much lower levels isolation and diversification of endemic populations, as of genetic diversity, but greater levels of genetic dif- well as recent human-mediated introductions that cor- ferentiation from each other and from adjacent marine roborate historic reports from early European explorers populations than is typical of marine Atlantic cod of Alaska. Managers now have a framework to prior- populations. Their isolation from one another and their itize the removal of non-native (introduced) popula- relatively low population sizes and small geographic tions which are impacting nesting birds, while leaving range are important considerations for future harvest long-established endemic populations intact. and management strategies. importance of applying evolutionary principles to detect 17.3.4. Tracking the invasion of species and study isolated or insular populations (Arnason et al. 2009, Jakobsdottir et al. 2011). The contemporary northwards expansion of sub-Arctic as well as human induced invasive alien species into the Parasites also reveal complex histories for faunal assem- Arctic could have profound effects on native flora and blages distributed in archipelago systems, and more gen- fauna through a variety of processes (e.g. competitive erally (Koehler et al. 2009, Hoberg et al. 2012a, 2012b) displacement, predator-prey interactions, hybridiza- they can provide clear signals about the origins, distribution and host-pathogen interactions; see also Lassuy & tions and history for host species (e.g. Brooks & Hoberg Lewis, Chapter 16). Rapid climate change could affect 2000). Unequivocal genetic signatures can be used to these interactions by expanding the ‘climate envelopes’ of demonstrate (1) endemic populations of hosts, (2) per- more southerly-distributed species and/or by reducing sistence of parasite lineages and species in the absence the habitat suitability of native species (Stachowicz et al. of ancestral hosts, and thus historical evidence of wider 2002, Walther et al. 2002). The possibility that popula- ranges occupied by a host species, or (3) introduced pop- tions of Pacific salmon Oncorhynchus spp. that are found ulations. Further, such signatures reveal historical inter- within the species’ western Arctic distribution may be actions between host lineages and species (e.g. ecological temperature-limited (Craig & Haldorson 1986) fuels relicts, patterns of contact, sympatry, extirpation and ex- concern that Arctic warming could cause north- and tinction). All have implications for wildlife management eastward range expansion, where they could negatively and conservation. Genetic signatures for parasites reveal impact native anadromous and freshwater fishes (Reist et host history at fine temporal scales, and the interaction al. 2006; see also Christiansen & Reist, Chapter 6). of historical and anthropogenic factors. For example, phylogeographic analyses demonstrate episodes of inva- Contemporary host-pathogen assemblages across the Arc- sion for host parasite assemblages in martens Martes spp. tic represent complex mosaics that have been structured and other mustelids and carnivores from Eurasia into by historical episodes of biological invasion, primarily North America (e.g. Zarlenga et al. 2006, Koehler et al. from Eurasia into North America over the Quaternary 2009). Intricate patterns of geographic colonization and (e.g. Rausch 1994, Hoberg 2010, Hoberg et al. 2012a). development of mosaic faunas composed of endemic and Invasive processes are evident for pathogens of free- introduced species reveal the disparate mechanisms that ranging ungulates, carnivores, rodents and a diverse array contribute to faunal structure in space and time (Hoberg of parasites that are transmissible from animals to people 2010, Hoberg et al. 2012a). (e.g. Kutz et al. 2004, 2009b). Secondarily, natural and human-facilitated invasion continues to structure this Prior hypotheses related to complex Arctic systems were fauna. It is important to understand the implications of posed before modern molecular methods were avail- such invasions for geographic expansion under a regime able. New methods now allow us to test these hypotheses of climate change and ecological perturbation (e.g. related to degree of isolation in ways not previously Hoberg et al. 2008, Laaksonen et al. 2010). Molecular possible allowing a more robust picture of diversity, in genetics provides the framework and analytical tools to addition to the biotic and abiotic drivers which structure identify sources for invasions and introductions, the num- the biosphere. Thus, molecular methods have altered our bers and timing of events, genetic variability associated view of the world, particularly relative to temporal scale with source and founder populations, successful estab- and landscape level processes that drive isolation and lishment and subsequent patterns of dissemination (e.g. ultimately endemism. Hoberg 2010). 580 Arctic Biodiversity Assessment

17.3.5. Identifying emerging pathogens DUs in a conservation context (e.g. Fraser & Bernatchez 2001, COSEWIC 2012). Given the commonality with Molecular and phylogeographic data are also instrumen- which cryptic phylogeographical variation is resolved tal in recognizing and documenting the introduction and within sub-Arctic taxa (Bickford et al. 2007), a similar emergence of pathogens and diseases in space and time. level of effort directed across Arctic landscapes would Molecular data allow the exploration of diversity in both probably reveal considerable variation that would con- a geographically extensive and site intensive manner that tribute to ESU/DU identification in Arctic taxa. was not possible previously (e.g. Jenkins et al. 2005, Kutz et al. 2007). For example, our understanding of the di- Genetic data have contributed more commonly to the versity and distribution of tissue dwelling and pulmonary resolution of shallower (in terms of inferred times of nematodes (protostrongylids) in ungulates (e.g. caribou, divergence) population structure and ‘management units’ muskoxen and wild sheep) depended on laborious and of- (MUs; e.g. Moritz 1994), particularly in fishes and some ten logistically difficult necropsy of mammalian hosts for terrestrial and marine mammals (e.g. Paetkau et al. 1995, recovery and definitive identification of adult parasites; 1999, Brown-Gladden et al. 1997, Harris & Taylor 2010). larval stages of parasites could not be reliably identified. Other management-related applications of conservation The development of species-specific markers for molecu- genetic methods are only beginning in Arctic contexts. lar identification has dramatically changed the process for For instance, landscape genetics is a fast growing research survey and inventory, and now substantial numbers of activity that attempts to understand how underlying land- potential host animals can be surveyed across broad geo- scape features structure populations genetically (Manel graphic ranges simultaneously to provide a rapid picture et al. 2003). One application of landscape genetics is of the distribution of pathogens and disease (Hoberg et al. to enable predictions about how changes to landscapes 2008). Necropsy is no longer required, and assessments may impact demographic and genetic connectivity. The of diversity can be obtained by sampling and sequencing importance of sea ice to life history attributes of many individual larval nematodes which can be simply and reli- Arctic animals, for example, is reflected in its role in ably recovered from fresh fecal samples. These methods driving the evolution of population structure (e.g. Geffen facilitate rapid diagnostics and concurrently provide the et al. 2007). basis for phylogeographic analyses to explore historical and contemporary processes as determinents of faunal structure. Molecular markers are increasingly important 17.4. ADVANCES IN TECHNOLOGY in tracking environmental perturbation linked to climate change that rapidly alters the host and geographic ranges AND ANALYTICAL METHODS for an array of parasites in both free ranging vertebrates and humans (e.g. Polley & Thompson 2009). 17.4.1. New technology

17.3.6. Threatened and endangered species, One of the roles of conservation genetics is to understand the adaptive potential of species exposed to climate ESUs and MUs change and anthropogenic challenges. Genomics ap- Effective conservation of the contemporary character- proaches allow the mapping of associations between istics and future potential of biodiversity requires an adaptive genome regions and environmental gradients in understanding of major units within species. Tradition- space and time. Recent advances in genomics will revolu- ally, the recognition of such diversity has taken the form tionize genetic analysis of natural populations. Previously, of subspecies, but since the 1980s other descriptors such population genetics was confined to dozens of micro- as ‘evolutionarily significant units’ (ESUs; Ryder 1986) satellite markers or gene variants. New genomic and or ‘designatable units’ (DUs; Green 2005, COSEWIC transcriptomic techniques produce much larger amounts 2010) have been emphasized. of data that are well suited to solve problems in conservation genetics regarding the basis of inbreeding depression Relatively little work has focused on identifying ESU/ and adaption. These techniques include marker-based DUs within Arctic habitats, although such units are often genotyping, reduced-representative sequencing (Alts- resolved as part of other biogeographic or population chuler et al. 2000) and whole genome/transcriptome genetic analyses. For instance, Brunner et al. (2001) used sequencing (Fig. 17.2). Single nucleotide polymorphisms mtDNA to identify five phylogeographic lineages within (SNPs) are by far the most common source of genetic Arctic char Salvelinus alpinus across its Holarctic range. In variation and valuable as markers for genetic map con- some cases, these lineages were associated with distinct struction, modern molecular breeding programs and subspecific designations, but in other cases not. Holder quantitative genetic studies. SNPs are readily mined & Montgomerie (2004) used genetic data to identify up from genomic DNA or cDNA sequence obtained from to six ESUs in the rock ptarmigan Lagopus mutus. Because individuals having two or more distinct genotypes. ‘Next- these lineages are thought to have arisen via isolation and generation’ DNA sequencing technologies that utilize subsequent dispersal from distinct glacial refugia, their new chemistries and massively parallel approaches have genetic characteristics mark historical events that are part enabled DNA sequences to be acquired at high depths of of each taxon’s biotic heritage. Such historical groupings coverage faster and for less cost than traditional sequenc- often form one of the key criteria for identifying ESU/ ing. For example, researchers can now address previously Chapter 17 • Genetics 581 intractable questions in ecology and evolution with the ants. Genome scans will prove useful in assessing genetic aid of next-generation sequencing of ancient DNA pre- diversity, estimating functional genetic variation and served in permafrost sediments (Sønstebø et al. 2010). fitness, and monitoring and managing inbreeding depres- Restriction site associated DNA sequencing (RAD-Seq) sion to restore populations. For species reintroductions, is a powerful new method for sequencing and detection genomics also provides insight into appropriate source of SNPs across genomes of many individuals (Allendorf populations (see reviews by Primmer 2009, Allendorf et et al. 2010, Baxter et al. 2011). This approach has broad al. 2010, Avise 2010, Ouborg et al. 2010). The quest to potential for genotype-phenotype association mapping, characterize genetic diversity in the Arctic should also be phylogeography and population genetics of non-model approached through application of metagenomics, where species with no genome sequences available. Population multiple taxa are combined in a single sequencing assay genomic approaches allows us to identify genes involved (deLong 2009) or environmental DNA (eDNA) screen- in adaptive traits without prior information about which ing of soils or aquatic environments (Jerde et al. 2011). traits are important in the species in question (Allendorf The microbial community in the Arctic largely remains et al. 2010, Stapley et al. 2010, Ogden 2011). unexplored and might serve as a key factor in monitoring efforts (see Lovejoy, Chapter 11). A promising aspect of applying genomic tools to conservation is to identify signatures of selection in space and 17.4.2. New theory and analytical approaches time, to provide insights into local adaption and adaptive responses to changes in environment (Oleksyk et Advances in bioinformatic theory and analytical ap- al. 2010). Adaptive loci have been identified that show proaches (Knowles 2009), along with new software extremely high genetic divergence between populations and increased computing power, have all substantially of marine fish, while structural loci show no evidence of changed our ability to make inferences about the biology divergence (Waples 1998, Nielsen et al. 2009). Iden- of wild organisms based on the increased accessibility tification of individual loci with major adaptive effects of genomic data. Coalescent theory, for example, is an raises the possibility of rescuing specific genetic vari- extension of classical population genetics that builds on

Figure 17.2. Molecular genetics can be used to study functional genes that are important in responding to environmental change or to identify individuals, and then determine relationships between individuals, populations (represented here by orange boxes), metapopula- tions (turquoise boxes) or species (blue boxes). We explore how species have responded to change in the past (such as vicariant events that split larger groups into smaller groups), so that we can forecast how species will respond to changes in the future.

Applying molecular genetics in the Arctic Application (taxonomic level)

• Ancestry-divergence (A, B, C, D) • Hybridization (C, D) • Species identi cation (D) • Individual identi cation (A) • Population structure (B, C) • Eective population size (B, C, D)

Vicariant event or other process

Geographic or other barrier D. Species

C. Metapopulation

B. Population g Genomics g g equencin cs/genomics s Gene sequencing Gene genotyping P anscriptomi SN SNP genotypin μsat genotypin Tr

A. Individual Tools: Tools: Neutral markers Natural selection Functional markers 582 Arctic Biodiversity Assessment the Fisher-Wright model (Kingman 1982, Wakely 2008). Because specimens are often used by multiple and diverse This approach has provided insight into topics as diverse research projects, they automatically integrate and tie as human migration into the Americas (Hey 2002), dis- together distinct disciplinary approaches. Continued ease persistence and emergence (Rosenberg & Nordborg development and expanded financial support of these 2002) and beluga whale population structure (O’Corry- permanent collections is essential to future efforts to Crowe et al. 1997). Approximate Bayesian Computation monitor Arctic biodiversity. is another powerful analytical approach recently developed to estimate historical parameters from genetic vari- 17.5.1.1. Build European, Asian and North American ation and compare quantitatively alternative demographic tissue archives scenarios (Beaumont 2010). One example of a collection that was established to archive and provide the materials necessary to a broad 17.5. RECOMMENDATIONS AND spectrum of investigators is the University of Alaska Museum of the North’s Genomic Resources Facility. CONSERVATION MEASURES This cryogenic collection contains tissue samples from > 85,000 voucher specimens of mammals, birds, fishes, Within the past 25 years, molecular genetics has radically plants and insects. In Norway, a DNA bank focused on shifted our perspective on biodiversity on the planet, circumpolar vascular plants has been established at the with innovations continuing to increase our ability to rap- Natural History Museum, University of Oslo, currently idly characterize and investigate the processes responsible containing close to 100,000 tissue samples and frozen for life. However, a number of issues continue to hamper DNA extracts. Several other museums also hold large our ability to fully exploit new technology. Arctic tissue collections. The Alaska Marine Mammal Tis- sue Archive Program is now housed at the US National 17.5.1. Call for immediate development of Marine Mammal Tissue Bank archives and provides protocols for the long-term storage of tissues from marine freely available, specimen-based mammals. The Tissue Bank uses a series of biomonitoring archives sites to collect tissues on specific indicator species (e.g. Arctic physical scientists have ambitiously developed a northern fur seal Callorhinus ursinus), animals from mass geographically extensive monitoring infrastructure to strandings and mortality events. acquire vast quantities of data across terrestrial, oceanic and atmospheric systems related to climate change. 17.5.2. Expand biodiversity informatics Parallel resources necessary to develop infrastructure for monitoring biological systems in the Arctic continue Explosive growth of information about both biotic and to lag, limiting the integration of aspects of biological abiotic components of the environment has created a and physical processes. Perhaps the greatest limitation to need to develop interconnectivity between large on-line effective use of genetic approaches to monitoring Arctic databases so that we can rapidly and accurately assess faunal and floral response to changing climate is the lack changing conditions. Examples of such efforts are the of biological specimens and, concurrently, the lack of co- Global Biodiversity Information Foundation (www. hesive protocols for acquiring and sharing synoptic data gbif.org) and VertNet (www.vertnet.org); efforts that and samples from wild populations. The development facilitate the mobilization, access, discovery and use of and implementation of a comprehensive strategy to build information about organisms over time and across the archival resources (Fig. 17.1) that represent key faunal planet. Permanent archival collections, as the foundation and floral populations across the Arctic should be a high for informatics, represent critical historical baselines and priority. Collaborations among rural communities, local, self-correcting records for the distribution and structure regional, national and indigenous managers, subsistence of biodiversity. hunters and trappers, field biologists and museum archi- vists to form networks to acquire biological information 17.5.2.1. Connect GenBank, EMBL and DDJB to would significantly stimulate efforts across biological Archives disciplines. Especially critical is the need to build much more robust archival collections for specimens and GenBank (www.ncbi.nlm.nih.gov), along with the tissues that document and form the basis for monitoring European Molecular Biology Laboratory Nucleotide changes in the complex biota that includes both free-liv- Sequence Database (EMBL) and the DNA Data Bank of ing and parasitic organisms. Non-invasive methods of Japan (DDJB), are the largest repositories for the vast recovering DNA have improved tremendously and are amount of genetic information on wildlife populations often the most appropriate for studies of endangered in the Arctic. GenBank for example, began in 1979 and species. Unfortunately, there are no coordinated or sus- now contains publicly-available nucleotide sequences for tained efforts to archive and share such samples among more than 300,000 organisms. The amount of informa- investigators, so their value has been limited. In contrast, tion in GenBank doubles about every 30 months with specimens in natural history museums remain the highest 95 billion nucleotide bases from more than 92 million quality source of spatially and temporally extensive individual sequences represented in 2008 (Benson et al. samples available for Arctic geneticists and managers. 2009). However, only a fraction of the genetic infor- Chapter 17 • Genetics 583 mation in GenBank is from wild Arctic populations history collections (e.g. ARCTOS, arctosdb.wordpress.com) and less is associated with a specific geographic locality or long-term environmental monitoring efforts (e.g. (i.e. georeferenced); however, this situation is changing. Longterm Ecological Research). The data should be Without the georeferenced tag that museum specimens available to policy makers and central to educational directly provide, genetic data have limited applicability to initiatives in high schools and undergraduate university questions related to changing environmental conditions. classes to engage the next generation more immediately With regard to genetic analyses of Arctic species, there in hands-on training efforts. Because the Arctic is geo- remains an urgent need to implement a ‘gold standard’ graphically remote to most humans, portals that provide for future development of genetic databases, because rep- interpretation of the science as well as ready availability lication and repeatability are essential precepts of good of data to teachers and the general public are essential to science. In the case of GenBank and related databases, the building a constituency who will appreciate and respond gold standard would be to ensure that genetic sequences to the changes currently underway at high latitudes. The for Arctic species are backed by voucher specimens that value of the vast environmental data held and managed are permanently archived in museums and thus available by scientific programs, such as those in natural history for future expansion and proofing of genomic databases collections, will continue to rise in the future. Online da- (Federhen et al. 2009). tabases can form the basis for an interactive platform to address questions about the patterns of biodiversity and the impact of environmental change on varying temporal 17.5.2.2. Connect GenBank (Genomics) to GIS and spatial scales, but only if there is a clearer focus on applications these endeavors. Genetic and ecological niche models (Peterson 2001) can be combined to infer the historic distribution of a 17.5.3. Identify, survey and monitor genes species to provide insight into the genetic structure of contemporary populations (Knowles et al. 2007), includ- that influence fitness ing Arctic species (Hope et al. 2010, 2011). Ecological We are just beginning to integrate ecological genetics with niche models use georeferenced, voucher specimens to genome-scale studies to explore how variation at the level determine the environmental parameters that govern of the DNA molecule determines phenotypes of Arctic species distributions. These models then provide hypoth- organisms (Höglund 2009). We need to incorporate our eses that can be tested using genetic approaches, includ- knowledge of evolutionary and ecological processes of ing the prediction of future response of wild populations endangered populations in the Arctic, so that a molecular to changing environments. Only a small subsection of genetics approach forms the basis for effective conserva- genetic databases represent georeferenced specimens, so tion planning and action. For example, studies have shown a sustained effort to increase the quality and applicability that the loss of genetic diversity both in neutral (mtDNA) of these databases is needed. and functional genes (the major histocompatibility complex, a gene family involved in immune response) has been observed in Arctic fox from the Komandorski Islands, 17.5.2.3. Stimulate emerging pathogen investigations particularly in the endangered subspecies V. l. semenovi from through integrated inventories Mednyi Island (Dzikia et al. 2007). Comprehensive survey and inventory for vertebrates, invertebrates, plants and associated pathogens using newly 17.5.4. Monitor response to climate change developed molecular-based methods allow for geographically extensive and site intensive explorations of diversity (neutral and functional variation) (e.g. Hoberg et al. 2003, Cook et al. 2005, Jenkins et Assessment of historical and contemporary connec- al. 2005, Kutz et al. 2007, Hoberg et al. 2008). These tivity among populations provides a starting point for surveys establish comparative baselines against which en- elucidating this basic response to changing conditions. vironmental change may be assessed. Surveys are further An Arctic-wide, multispecies monitoring and archival enhanced by linkage to integrated archival collections and program across trophic levels could use sentinel or focal informatics systems for both free-living organisms and (Hodkinson, Chapter 7) species across the taxonomic an array of pathogens. Such integrated frameworks for spectrum to assess changes in both neutral and function survey and inventory are requisite to rapidly identify pat- molecular markers (Weider et al. 2010). These species terns of changing distribution and emergence of diseases should have widely different ecological characteristics associated with pathogens (e.g. Brooks & Hoberg 2006, and may respond differentially to climate warming. Hoberg 2010, Hoberg et al. 2012a). There is an urgent need to increase survey efforts in the Arctic. Adaptive genetic variation among populations provides insight into the evolutionary potential of populations (Palsbøll et al. 2006, Schwartz et al. 2007), helps set the 17.5.2.4. Develop educational interfaces and portals stage for conservation strategies (Hansen 2010) and can for Arctic databases provide input to the definition of ESUs (Waples 1991). The urgency of making large online databases more acces- Assessment of functional genetic divergence (Box 17.10) sible cannot be overemphasized. These databases include or local adaptation, however, has proved elusive. Import- those associated with genomic data (via GenBank), natural ant gene expression differences exist in Atlantic salmon 584 Arctic Biodiversity Assessment

Box 17.10. Characterizing functional genes

Unfortunately, the importance of certain functional studies of fitness components failed to uncover any adap- genes is not always clear-cut, requiring species-specific tive advantage associated with either morph, geese show analyses. The melanocortin-1 receptor gene (MC1R) is strong mating preference based on the color of their responsible for melanic differences in at least two Arctic parents, leading to assortative mating (Cooke et al. 1976, species (Mundy et al. 2004), the lesser snow goose Chen c. 1995). Single non-synonymous changes are perfectly as- caerulescens and the parasitic jaeger Stercorarius parasiti- sociated with the presence of melanism in both the goose cus, where this derived trait is apparently under selection and jaeger, although different substitutions are involved (Mundy 2005). In the parasitic jaeger of the Shetland (Mundy et al. 2004). The relationship between polymor- Islands, UK, males with melanic morphs breed earlier in phism at MC1R in other northern avian species, however, the season than males with pale morphs, but pale morph is not straightforward; Hull et al. (2010) failed to uncover males may breed at an earlier age. Lesser snow geese a relationship between polymorphism in the MC1R gene show an approximate east-west cline in their Nearctic between dark and light morphs of temperate and boreal breeding distribution in frequency of pale or dark morphs, red-tailed hawks Buteo jamaicensis in northern North with blue morphs most common in the east. Although America.

Salmo salar that are associated with distinctive ecological For populations on the brink of extinction, a detailed conditions, suggesting an important potential role for map of genetic structure is crucial for conservation ef- transcriptomes analyses in defining units for conservation forts including a blueprint for rescue or restoration (He- (Tymchuk et al. 2010). Like next-generation genomics drick 2005) in the face of changing climate and increas- technologies, burgeoning next-generation transcriptom- ing anthropogenic impacts in the Arctic. Because natural ic technologies will revolutionize our understanding of selection can rapidly accelerate the rate of introgression gene expression in natural populations. of certain regions of the genome, the source of the introduced individuals must be carefully chosen (Fitzpatrick et 17.5.5. Management and forensic al. 2010). Assisted colonization is reintroducing species to locations where they do not now occur (Hoegh-Gul- applications dberg et al. 2008, but see Tallmon et al. 2004); such also may involve the unintended translocation and introduc- 17.5.5.1. Ensure rigorous identification tion of parasites with their hosts (e.g. Hoberg 2010, Hoberg et al. 2012). Rapid identification of organisms is important to a number of management goals. DNA barcoding is gaining wide Petit et al. (1997) noted that conservation priorities attention as it uses standardized sequences that can be should consider genetic uniqueness as well as diver- obtained relatively cheaply as a molecular diagnostic tool sity. They suggested that a measure of ‘allelic richness’ for species-level identification. Importantly, this effort provides an unbiased estimate of diversity and unique- has extended molecular approaches into educational ness. Taylor et al. (2011) applied this technique to rank efforts and to a number of new applications including populations of rainbow trout Oncorhynchus mykiss in terms forensic identification. These and other markers com- of total genetic diversity (a combination of genetic diver- monly used in population genetics and phylogeographic gence between populations and genetic diversity within studies of Arctic species can be used to address specific populations). These genetic measures of diversity were conservation and management goals, and include the use combined with measures of morphological diversity (as a of (1) polymorphic genetic markers such as microsatel- proxy measure of adaptive variation) to rank populations lites in ‘genetic tagging’ and other non-invasive efforts to in terms of conservation priority. Similar approaches estimate population size and life-history parameters such have been developed to rank species in terms of phylo- as survival and mating strategies (Schwartz et al. 2007), genetic distinctiveness (Redding & Mooers 2006) and (2) molecular techniques to determine the sex in species geographic areas in terms of species richness or biogeo- with little sexual dimorphism (Griffiths et al. 1998), and graphic endemism (Myers et al. 2000), yet they have not (3) genetic markers to determine the species and indi- been applied within the context of Arctic conservation. viduals involved in human-animal conflict to help identify specific animals involved in attacks and absolve those that are not (Farley et al. in press). 17.6. CONCLUSIONS In this review we have touched on several topics for 17.5.5.2. Provide framework for assisted colonization which non-commercial genetic approaches are provid- or genetic restoration ing key insights into changing conditions in wildlife and Climate change is likely to amplify the negative effects of plant communities in the Arctic. We have not addressed human exploitation and mismanagement in many cases. concerns about genetic prospecting and commerciali- Chapter 17 • Genetics 585 zation of genetic resources in the Arctic. Instead, our REFERENCES overview of not-for-profit genetic approaches in the Arctic emphasizes that an understanding of the influence Abbott, R.J. & Brochmann, C. 2003. History and evolution of the of deeper (evolutionary) time in structuring diversity is Arctic flora: In the footsteps of Eric Hultén. 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