genetics, evolution, and phylogeography of...

ALCES VOL. 40, 2004 MOOSE GENETICS - HUNDERTMARK AND BOWYER

103

GENETICS, EVOLUTION, AND PHYLOGEOGRAPHY OF MOOSE

Kris J. Hundertmark1 and R. Terry Bowyer2

1Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks,Fairbanks, AK 99775, USA; 2Department of Biological Sciences, Idaho State University, Pocatello,ID 83209, USA

ABSTRACT: Early studies of genetic variation in moose (Alces alces) indicated little variation.Recent studies have indicated higher levels of variation in nuclear markers; nonetheless, geneticheterogeneity of moose is relatively low compared with other mammals. Similarly, variation inmitochondrial DNA of moose is limited worldwide, indicating low historic effective population sizeand a common ancestry for moose within the last 60,000 years. That ancestor most likely lived incentral Asia. Moose likely exhibit low levels of heterogeneity because of population bottlenecksin the late Pleistocene caused by latitudinal shifts in habitat from recurrent climate reversals. Anorthward movement of boreal forest associated with the end of the last ice age facilitated thenorthward advance of Asian populations and colonization of the New World, which occurred asa single entry by relatively few moose immediately prior to the last flooding of the Bering land bridge.Despite suffering serial population bottlenecks historically, moose have exhibited a notable abilityto adapt to a changing environment, indicating that limited neutral genetic variation may not indicatelimited adaptive genetic variation. We conclude that morphological variation among mooseworldwide occurred within a few thousand years and indicates that moose underwent episodes ofrapid and occasionally convergent evolution. Genetic change in moose populations over very shorttime scales (tens or hundreds of years) is possible under harvest management regimes and thosechanges may not be beneficial to moose in the long term. Modeling exercises have demonstratedthat harvest strategies can have negative consequences on neutral genetic variation as well asalleles underpinning fitness traits. Biologists should consider such outcomes when evaluatingmanagement options.

ALCES VOL. 40: 103-122 (2004)

Key words: adaptation, Alces, convergent evolution, moose, mtDNA, phylogeography, Pleistocene,range expansion

Genetics have long had a central role inbiological investigations, and provide ana-lytical tools that are applicable across abroad spectrum of investigation. For in-stance, genetic analysis can provide insightsinto such diverse investigations as evolu-tionary histories of species (Avise et al.1987, 2000), interactions and relationshipsamong populations (Blundell et al. 2002) orindividuals (Quellar et al. 1993), evaluationof the success of specific management ac-tions (Vernesi et al. 2002), population andbehavioral ecology (Scribner and Chesser2001), and food habits (Symondson 2002).

Recent advances in collection and analysisof genetic data have facilitated more re-fined approaches to evolutionary and popu-lation genetic questions, and our under-standing of moose biology has benefited asa result of those advances.

Evolution and taxonomy of moose (Alcesalces) have been reviewed previously(Peterson 1955; Groves and Grubb 1987;Geist, 1987a,b, 1998; Sher 1987; Lister 1993;Guthrie 1995; Bubenik 1998; Bowyer et al.2003) and have encompassed aspects ofbehavior, morphology, paleontology, andgenetics, but no review has dealt specifi-

HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004

104

cally with genetics. In this review, our goalis to provide an overview of older studieswhile focusing on recent advances in genet-ics and phylogeography (see definition inAppendix 1) of moose and the insights theyprovide.

The broad scope of genetic and evolu-tionary investigations in species biologywould make a complete review of all studiesdisjointed. Yet, approximately half of allpublished studies of moose genetics havebeen published since the comprehensivetreatise “Ecology and Management of theNorth American Moose” (Franzmann andSchwartz 1998) was compiled; thus, wewere compelled to present the most com-plete review possible. In an effort to presenta cogent summary of all relevant studies,we have divided this review into 3 parts: (1)assessing genetic diversity, where we re-view the different types of markers exam-ined in studies of moose genetics and theconclusions drawn from those studies; (2)moose evolution and phylogeography, wherewe examine the evolutionary descent ofmoose and processes that have shaped thegenetic variation and structure observedtoday; and (3) genetic effects of harvest,which reviews a small but important body ofwork composed of management-basedmodeling that examined effects of variousharvest regimes on population and geneticmeasures.

ASSESSING GENETIC DIVERSITYOne potential difficulty in discussing

genetic analyses is the use of specializedterminology. To avoid uncertainty and en-hance understanding, we provide a briefglossary of terms used in this review (Ap-pendix 1). Terms defined in the glossaryare highlighted in bold in the text at their firstusage.

The Allozyme EraFirst reports of genetic investigations of

moose were published by Braend (1962,cited by Gyllensten et al. 1980), Nadler etal. (1967), and Shubin (1969, cited byGyllensten et al. 1980), wherein those au-thors examined electrophoretic variation inproteins from blood serum; no variation inthose genetic markers occurred in Scandi-navia, North America, and central Russia,respectively. The first study to report ge-netic variability was Ryman et al. (1977),who examined 1,384 moose from 3 areas ofSweden for polymorphism at 23 allozymeloci. That study reported only 1 locus to bepolymorphic, however, and only in 1 region.Although they suspected that allele fre-quencies varied geographically within the 1variable region, the difference was not sta-tistically significant. Those authors con-cluded that genetic drift associated with asevere population bottleneck (reduction inpopulation size) in Sweden in the 19th cen-tury was a probable cause of the observedlack of diversity. Wilhelmson et al. (1978),examining variation in serum proteins, notedno differences between Canadian and Eu-ropean moose. From that evidence, theyconcluded that moose populations on sepa-rate continents had not undergone signifi-cant genetic drift despite being separatedfor thousands of years, implying that effec-tive population sizes of moose populationshistorically had been large.

Wilhelmson et al. (1978) also proposedthat historic population bottlenecks in Swe-den had not been severe enough to have hadan effect on genetic diversity of moose.Gyllensten et al. (1980) conducted exten-sive screening of a transferrin locus frommoose across Fennoscandia and detected asingle polymorphism occurring in Norway,Sweden, and Finland. Nonetheless, the poly-morphism was present in only 6 of 16populations and the uncommon allele neverexceeded 6% in any population. The au-thors presented differences in frequency ofthe uncommon allele as evidence of differ-


105

entiation of populations geographically, sup-porting observations of Ryman et al. (1977).Reliance on the occurrence of a single rarepolymorphism to demonstrate populationsubdivision, however, is tenuous at best.

Those early studies and others createdan impression among some biologists thatcertain species, including moose, possessedlittle genetic variation across the genome.Hypotheses explaining this in evolutionaryterms were proposed. Selander andKaufman (1973) proposed the environmen-tal-grain hypothesis, which stated that large,highly mobile animals exhibited less geneticvariability than small, sedentary species.That hypothesis further stated that highlymobile mammals would exhibit greater ho-mogeneity across large areas than moresedentary forms. Other hypotheses pro-posed that r-strategists were less variablethan K-strategists (Harrington 1985), ge-netic heterogeneity was greater in speciesinhabiting broad arrays of habitats com-pared with habitat specialists (Nevo 1978),or that northern cervids inhabiting borealforests were less variable than their rela-tives to the south (Smith et al. 1990).

Analyses of 23 allozyme loci in > 700individuals representing 18 moosepopulations in Scandinavia were required toreveal extensive genetic variation in moose(Ryman et al. 1980). Those authors refutedthe environmental-grain hypothesis, con-cluding that large mammals in general, andlarge cervids in particular, are not naturallymonomorphic; previous studies of moosehad examined too few loci or individuals todetect variation. Nonetheless, those au-thors noted that genetic variability in moosewas somewhat less than that observed inmany other species of mammals (Nevo1978), but that genetic drift due to smallhistoric population size was a more likelyexplanation than any specific evolutionarystrategy. Thus, genetic drift was once againproposed as being an important factor in

determining the structure of genetic diver-sity. In another comprehensive study,Chesser et al. (1982) examined 1,169 indi-viduals from 4 regions in Sweden for asingle polymorphic locus and reported vari-ation in allele frequencies among those re-gions and, perhaps more importantly, sig-nificant variation within 1 of those regions.Detecting variation at geographic scalessmall enough to be considered within asingle population illustrated that structure ofmoose populations existed at scales smallerthan previously imagined, and that vagilitywas not inconsistent with genetic structur-ing.

The most recent study of allozyme vari-ation in moose reported extensive variationin a moose population in Alaska(Hundertmark et al. 1992). The level ofgenetic diversity observed was greater thanthat reported elsewhere in moose and wassimilar to levels observed in white-taileddeer, a species known for extensive allozymediversity (Smith et al. 1984). Hundertmarket al. (1992) hypothesized that lesser levelsof variability described in moose from Scan-dinavia and other regions of North Americawere attributable to glacial history. Allother moose populations studied to that pointoccurred in previously glaciated terrain thatwas colonized by moose after retreat ofPleistocene ice sheets. Colonization ofpreviously glaciated areas could have re-sulted in serial founder events that reducedgenetic diversity (Sage and Wolff 1986).Hundertmark et al. (1992) argued thatAlaska could have served as a refugium formoose in which genetic diversity could havebeen maintained because of a large effec-tive population size.

Assessing Variation at the SequenceLevel

The first investigation of highly poly-morphic molecular markers in moose docu-mented 4 alleles in a microsatellite-like


106

locus in 17 individuals from Sweden (Ellegrenet al. 1991). Eight genotypes were re-ported, which represented a heretofore un-thinkable level of polymorphism. Thoseauthors investigated the inheritance of thatlocus in a 2-generation pedigree and deter-mined that the alleles exhibited Mendelianinheritance. That study and others like itlaid the foundation for the explosion ofinterest in population genetics andphylogenetics based on molecular markersand the polymerase chain reaction (PCR;Mullis et al. 1986).

The advent of PCR represented one ofthe truly significant advances in the historyof molecular biology and genetics. Theprocess allows in-vitro amplification of DNAfrom miniscule amounts of starting material(theoretically as little as 1 molecule of DNA)to provide sufficient quantities for analysis.No longer were researchers required tosacrifice animals to acquire sufficient quan-tities and types of tissues for genetic analy-ses because any nucleated cell held thecomplete genetic complement of the indi-vidual. PCR offered unsurpassed access tothe genome, and researchers soon appliedthat to study genetics of moose.

Mikko and Andersson (1995) conductedthe first analysis of functional loci in ananalysis of variation in the major histocom-patibility complex (MHC) in moose fromSweden and Canada. The MHC is a familyof genes important in immune system func-tion, and low levels of diversity of MHCalleles have been interpreted as indicatorsof lost evolutionary potential and increasedsusceptibility to pathogens (Hedrick 1994).Mikko and Andersson (1995) noted verylow levels of MHC variation in both Swed-ish and Canadian moose. Moreover, thoseauthors documented similarity among allelesbetween continents and inferred the exist-ence of a bottleneck in an ancient mooselineage prior to divergence of European andCanadian lineages. Mikko and Andersson

(1995) applied a molecular clock to DNAsequence variation in the control regionof mitochondrial DNA (mtDNA) to datethe time of divergence of Swedish andCanadian moose, which they estimated at165,000-350,000 years ago.

The time since divergence of Europeanmoose also was analyzed by Ellegren et al.(1996). They assessed variation inminisatellite loci of Swedish moose andconcluded that normal evolutionary proc-esses could have generated the amount ofvariation observed within 10,000-50,000years after a severe bottleneck. Theirimplication, therefore, was that the estimateof divergence provided by Mikko andAndersson (1995) was too old by perhaps 1order of magnitude. Surprisingly, the twodata sets are not inconsistent; indeed, theyshow similar levels of variation consideringdifferences in evolutionary rates amongmarker types. The differences in estimatesfor date of divergence relate more to theevolutionary rate estimates used than todifferences in genetic variability.

Microsatellite loci were first describedfor moose by Wilson et al. (1997) and Røedand Midthjell (1998). Broders et al. (1999)demonstrated the utility of microsatellitesfor assessing population structure in mooseby assessing consequences of founderevents in Canada. Heterozygosity in 3populations founded by few individuals de-creased from 14-30% compared with thesource population. Broders et al. (1999), inassessing variability of moose on the islandof Newfoundland, Canada, demonstratedthat 2 consecutive founder events reducedheterozygosity by 46%. Although they couldnot discern any decrease in fitness as aresult of the decrease in diversity, the au-thors questioned the long-term viability ofthose moose populations. Nonetheless, lev-els of diversity in neutral microsatellite lociwere not indicative of diversity in functionalloci in moose (Wilson et al. 2003).


107

The FutureMicrosatellites have replaced allozymes

as the most widely used molecular markerfor assessing nuclear genetic diversity, andwill be the choice of geneticists for theforeseeable future (Bruford et al. 1996).There are problems, however, with analysisof microsatellites because the ways in whichthey mutate into new forms are not entirelyunderstood (Hancock 1999). In the future,a new type of analysis called single nucle-otide polymorphism (SNP, pronounced“snip”) may replace microsatellites for someapplications (Fries and Durstewitz 2001,Brumfield et al. 2003). This new technol-ogy allows a single nucleotide site to bequeried for presence of a particular nucle-otide and presence or absence can be con-verted to a binary code. Current technology(so-called “real-time PCR” and “DNAchips”) allows for fast and accurate exami-nation of many individuals and SNPs, butwe must await the development and char-acterization of marker loci before broadapplication of this new family of molecularmarkers can be considered.

MOOSE EVOLUTION ANDPHYLOGEOGRAPHY

Origins of Modern MooseMoose (Alces alces) are a young spe-

cies in the evolutionary scheme of largemammals. The genus Alces first appears inthe fossil record 2 million years ago(Thouveny and Bonifay 1984) and fossilsattributable to A. alces are first recordedapproximately 100,000 years ago (Lister1993). Those dates are very recent consid-ering that the subfamily Odocoileinae, towhich moose belong, diverged from otherdeer lineages 9-12 million years ago(Miyamoto et al. 1990).

Paleontological evidence indicated Eu-rope as the place of origin of the genusAlces (Lister 1993). The genus never wasdiverse, with only one species present in the

fossil record at any particular time. Yet, thespecies assumed to be the precursor to A.alces , the broad-fronted moose (A.latifrons) was distributed across Eurasiaand into northwestern North America for atime before becoming extinct in Beringia atthe end of the Pleistocene (Guthrie 1995).Thus, the widespread distribution of modernmoose and its immediate ancestor indicatea degree of evolutionary success despite apaucity of species diversity.

Up to 8 subspecies of moose are recog-nized worldwide (Fig. 1); 4 in Eurasia and 4in North America (Peterson 1955). Thatnumber is open to question, however. Geist(1987a, 1998) contends that there are 2predominant types of moose in the world:American and European, following the con-vention of Flerov (1952). To the formertype he assigns all North American mooseas well as eastern Asian subspecies A. a.burturlini and A. a. pfizenmayeri. Hebased his opinion primarily on morphologyand noted similar geographic divisions intaxonomy among reindeer and caribou(Rangifer tarandus) and red deer and NorthAmerican elk (Cervus elaphus; Geist 1998).He further contended that those morpho-logical types should correspond to subspe-cies designations. Therefore, Geist (1998)recognized A. a. alces of Europe and A. a.americana in eastern Asia and NorthAmerica. He also suggested that A. a.americanus has precedence undernomenclatural conventions as the propername for the east Asian-North Americansubspecies. He referred to A. a.cameloides in northern China, Mongolia,and southeastern Russia as part of a primi-tive fauna native to that region and recog-nized that subspecies as a valid taxon al-though he also refers to it as an American-type moose (Geist 1998:230).

The 2-types hypothesis is supported tosome degree by karyotype (Boeskorov 1996,1997) and some data on mtDNA (Mikko


108

Fig. 1. Approximate ranges of 8 subspecies of moose worldwide. A. a. a. = A. a. alces, A. a. p. = A.a. pfizenmayeri, A. a. c. = A. a. cameloides, A. a. b. = A. a. burturlini, A. a. g. = A. a. gigas, A. a.an. = A. a. andersoni, A. a. s. = A. a. shirasi, A. a. am. = A. a. americana, * = introduced populationin Newfoundland.

and Andersson 1995). Most Eurasian moosehave a karyotype of 2N = 68, whereasNorth American moose have 2N = 70. Thatdifference derives from a Robertsoniantranslocation of 2 acrocentric chromosomesinto a single metacentric chromosome orvice versa. Although that chromosomalpolymorphism originally was thought to sepa-rate Eurasian and North American moose(Groves and Grubb 1987), the 2N = 70 formwas recently discovered in eastern Asia

(Boeskorov 1996, 1997). Similarly, a lengthmutation (insertion-deletion, or indel) withinthe control region of mtDNA originally wasdescribed as discriminating between NorthAmerican and European moose (Mikko andAndersson 1995), but subsequent investiga-tions documented that indel in moose fromEastern Asia (Hundertmark et al. 2002b,Udina et al. 2002). Although the precisegeographic distributions of thosepolymorphisms in karyotype and mtDNA


109

length are not well described, they seem tocorrespond geographically with a zone ofintergradation in east-central Asia, similarto that proposed for American and Eurasiantypes of moose (Flerov 1952, Geist 1998).More work is needed to determine the ex-tent of that geographic correspondence andto determine if it coincides with subspeciesboundaries. Moreover, the question of re-productive viability of the two chromosomalraces must be addressed. Indeed, Boeskorov(1997) has proposed that the chromosomalraces are different species and Groves andGrubb (1987) have identified them as “semi-species.” We caution, however, that chro-mosome numbers may be a poor designatorof species among large mammals (Bowyeret al. 2000).

Hundertmark et al. (2002b) tested the2-types hypothesis by examining the distri-bution of genetic variance of mtDNA amongand within different hypothetical populationstructures. Those authors sampled moosethroughout their worldwide distribution andarranged them into either 2 groups (corre-sponding to the 2-types hypothesis) or 3groups corresponding to continent of origin(Asia, Europe, and North America). Theythen examined the distribution of geneticvariance within and among or betweengroups, predicting that the correct structurewould minimize within-group variation andmaximize among-group variation. Percent-age of total variation observed among the 3groups was slightly greater than variationbetween the 2 groups (61.5% vs. 58.1%),and variation among populations withingroups was minimized in the 3-group com-parison (21.6% vs. 28.8% in the 2-groupcomparison). Therefore, Hundertmark etal. (2002b) concluded that mtDNA dataprovided no support for a 2-type over a 3-type hypothesis. That finding can be visu-alized by a phylogenetic tree constructedfrom haplotypes originally reported byHundertmark et al. (2002b, 2003), which

shows North American moose as distinctfrom both Asian and European forms(Fig. 2).

Ancient Bottlenecks and the Mother ofAll Moose

Moose worldwide exhibit little varia-tion in a fragment of the mitochondrial cyto-chrome-b gene (Hundertmark et al. 2002a).Cytochrome b is useful for constructingmammalian phylogenies (Irwin et al. 1991)and a paucity of variation in moose indi-cated a recent common ancestry likely dueto a severe bottleneck that affected allextant lineages (Hundertmark et al. 2002a),which is in agreement with the findings ofMikko and Andersson (1995). Analysis ofvariation within the mitochondrial controlregion, which evolves at a much faster ratethan cytochrome b (Lopez et al. 1997), was

Fig. 2. Unrooted phylogenetic tree of moosepopulations and subspecies worldwide, withthe exception of A. a. pfizenmayeri, using FSTas the distance measure [data fromHundertmark et al. (2002b, 2003)]. Note thedistinct positions of the 3 Eurasian subspe-cies and North American moose, which do notsupport an hypothesis of 2 or 3 races of mooseworldwide.


110

Fig. 3. A phylogenetic tree of haplotypes of themitochondrial control region of moose. Sym-bols indicate region of origin, with black sym-bols indicating Asian origin. Distinct cladesor phylogroups are indicated on the right.From Hundertmark et al. (2002b).

necessary to reveal significant levels ofvariation in moose and subsequently geo-graphic patterns were revealed.

Control region haplotypes of moosecan be divided into 3 clades, or haplogroups(Fig. 3). The basal haplogroup (i.e., thegroup that diverges first from the base ofthe tree) is entirely Asian, which suggeststhat those are the oldest moose haplotypes.The two other haplogroups are primarilyEuropean and primarily North American,although some Asian haplotypes occur inboth. The distribution of haplogroups on aworldwide scale illustrates the age of con-tinental assemblages of haplotypes (Fig. 4).The Yakutia area contains moose from all 3haplogroups. The Russian Far East con-tains both European and Asian haplogroups,but not North American, and both Europeand North America contain only 1haplogroup each. Therefore, Yakutia canbe identified as the area from which allextant moose lineages were derived, i.e., it

is the oldest extant moose population thathas been sampled.

Yakutia probably was the center of asingle moose population during the last iceage, or at least was the location of the onlypopulation to provide descendants of mod-ern moose. Moose would have been re-stricted in their distribution because thecooler climate in Asia at that time wouldhave resulted in a shift of boreal foresthabitat to the south. That habitat could haveshifted only so far southward, because ofprominent mountains running east-west,which would have formed an effective bar-rier to further movement to the south (Hewitt1996).

During the last ice age, there were 2periods of maximum glacial advance, termedthe lower and upper pleniglacials. Thoseepisodes occurred at approximately 62,000and 20,000 years ago, respectively (Fultonet al. 1986). Boreal forest habitats in Asiawould have shifted to the south during thosecooling episodes and would have been com-pressed against the northern slopes of moun-

Fig. 4. Distribution of mitochondrial haplogroupsworldwide. Note that moose from the Yakutiaarea have the most diverse composition andthat moose from North America do not sharehaplogroups with moose from Russian FarEast.


111

59,000 and 14,000 years ago. When expan-sion times of moose are overlaid on a profileof global temperature change for the last iceage (Jouzel et al. 1987), population expan-sion is correlated with warming trends fol-lowing the pleniglacials (Fig. 6). Conse-quently, the evolution and geographic distri-bution of moose seems to have been af-fected substantially by climate change, par-ticularly climate reversals associated withthe late Pleistocene and early Holocene.

Coming to AmericaCronin (1992) analyzed subspecific vari-

ation in North American cervids using re-striction fragment length polymorphisms(RFLP) of mtDNA. Despite analyzing 32moose sampled from different regions ofNorth America, he documented no varia-tion among haplotypes from that continent.In comparison to other North Americancervids, the lack of variation among subspe-cies of moose was interpreted as an indica-

Fig. 5. Glacial coverage during the last glacialmaximum, superimposed on a map of present-day sea level. Note that the Bering land bridgebetween North America and Asia would havebeen exposed during the glacial maximum dueto lower sea levels. Names of major ice sheetsare provided.

tain ranges. During subsequent warmingintervals, moose habitat would have spreadto the north, allowing moose populations toexpand (Guthrie 1995). Unlike NorthAmerica, much of Eurasia was not glaci-ated during those periods (Arkhipov et al.1986), providing potential dispersal routesacross the continent (Fig. 5). The processof latitudinal shifts of range associated withepisodes of climate change results in de-creases of existing genetic diversity (Hewitt1996) and leaves characteristic signaturesin the genome of modern moose.

Moose in Eurasia underwent 2 distinct,recent population expansions (Hundertmarket al. 2002b). Any other historic populationprocesses preceding those expansions arenot detectable because low population sizeseliminated much of the genetic variationpresent in the pre-bottleneck populations,and hence no signature from those timesexists in the present genome. By applying amolecular clock to those expansion data,Hundertmark et al. (2002b) estimated thatthe expansions occurred approximately

160 140 120 100 80 60 40 20 0

2

0-2

-4

-6

-8-10

Thousands of years ago

Tem

pe

ratu

re d

i ffe

renc

e (C

º)

Fig. 6. Representation of mean global tempera-tures during the last 160,000 years relative tomean temperature in 1900. Negative tempera-ture differences indicate periods colder thantoday. The 2 glacial maxima of the last ice ageare indicated by arrows. Estimated dates ofmoose population expansion are indicated bydashed lines and correspond to periods ofwarming associated with glacial retreat andnorthward advance of the boreal forest inEurasia. Temperature profile adapted fromhttp://gcrio.ciesin.org/CONSEQUNCES/win-ter96/article1-fig3.html.


112

ity in composition of mtDNA haplotypes.As noted previously, North American sub-species are distinct from European andAsian subspecies (Fig. 2) and none of theAsian haplotypes in the North Americanhaplogroup were found in the Russian FarEast. All haplotypes found in the RussianFar East (Magadan Oblast) are restricted tohaplogroup 2 (Fig. 3), which contains allEuropean haplotypes. A likely colonizationscenario entails closely related moose fromcentral Asia colonizing both Europe andNorth America.

Lack of genetic similarity betweenmoose in Alaska and the Russian Far Eastis inconsistent with the scenario proposedby Hundertmark et al. (2002b) concerning acolonizing wave of moose traveling fromAsia to North America through Beringia. Asingle wave of moose colonizing NorthAmerica through Beringia would have leftgenetically similar populations on either sideof the Bering Strait after the Bering landbridge flooded. Yet, ages of subfossil re-mains of moose from North America indi-cate clearly that A. alces was present inAlaska prior to anywhere else on the conti-nent (Guthrie 1990, Hundertmark et al. 2003),unequivocally supporting an entry throughBeringia. One hypothesis that accounts forthis seeming paradox is that 1 or both ofthose populations underwent population bot-tlenecks shortly after the colonization ofNorth America, and have only recentlyreestablished populations in those areas,leading to the presence of different geneticlineages in each. Moose in the Russian FarEast show evidence of an expansion ap-proximately 1,200 years ago (Hundertmarket al. 2002b) and continue to expand theirrange toward the Bering Sea (Zheleznov1993).

Similarly, Alaskan moose show a sur-prising lack of mitochondrial diversity com-pared with moose elsewhere on the conti-nent (Hundertmark et al. 2003), which is

tion of a recent common ancestry, consist-ent with colonization of the continent afterthe retreat of ice sheets from the last iceage (Cronin 1992). Similarly, no variationwas detected within a fragment of cyto-chrome b in North American moose com-pared with slight variation in Eurasia(Hundertmark et al. 2002a).

Moose populations in North Americawere established as a result of a single entryinto the continent, and that entry occurredduring the population expansion of moose14,000 years ago at the end of the last iceage, just before the closure of the Beringland bridge (Guthrie 1995, Hundertmark etal. 2002b). A recent entry into NorthAmerica is the only conclusion that is con-sistent with limited variation in the mtDNAcontrol region both within North Americaand between North America and Eurasia.If moose had existed in 4 separate refugia inNorth America during the last ice age, assuggested by Peterson (1955), or had en-tered North America from Asia more thanonce, a more distant common ancestorwould be indicated. The timing of the entryis supported not only by genetic data butalso by the distribution of suitable moosehabitat at the end of the last ice age. Thecold, dry grassland habitat that prevailed inBeringia for most of the last ice age wasunsuitable for moose and was replaced byboreal forest only within the last 14,000years (Guthrie 1995).

Evidence from mtDNA variation alsoindicates that North American moose didnot originate in Beringia, as some havespeculated (Cronin 1992, Geist 1998), orrecolonize the Russian Far East from NorthAmerica (Coady 1982). Moose in NorthAmerica are not closely related to moose onthe western side of the Bering Strait (Rus-sian Far East). If those moose were oncepart of the same population recently sepa-rated by the flooding of the Bering landbridge, we would still expect to find similar-


113

indicative of a bottleneck notwithstandingthe moderate levels of allozyme diversityreported for Alaskan moose by Hundertmarket al. (1992). Diversity of mtDNA can bereduced to a much greater degree by abottleneck than diversity of nuclear DNAbecause mtDNA is 4 times more sensitiveto genetic drift due to its haploid, uniparentalmode of inheritance (Birky et al. 1983).Simultaneous bottlenecks in moose fromboth sides of the Bering Strait suggest awidespread causal factor. Recent studieshave found evidence of significant bioticeffects of climate reversals in Beringia af-ter flooding of the Bering land bridge (Elias2000, Mason et al. 2001, Anderson et al.2002). Those effects offer an intriguingmechanism for bottlenecks in Beringianmoose populations.

The greatest variation in mtDNA inNorth American moose occurs within therange of A. a. andersoni (Hundertmark etal. 2003). Alces a. shirasi from Coloradoexhibited no diversity and A. a. gigas and A.a. americana exhibited very little diversity.If the paucity of mitochondrial diversity inAlaska is due to a bottleneck and recentexpansion, those data would be consistentwith the serial-founder-events hypothesisof North American colonization(Hundertmark et al. 1992).

The pattern of colonization of NorthAmerica undoubtedly was influenced bythe retreating glaciers and may have hadsome effect on genetic structure(Hundertmark et al. 2003). Based on thereconstruction of the retreat of theLaurentide ice sheet by Dyke and Prest(1987), we offer the following scenario ofcolonization. At the last glacial maximum,the Cordilleran and Laurentide ice sheetscreated an effective barrier between east-ern Beringia (Alaska) and other parts of thecontinent (Fig. 5). As glaciers retreated, acorridor opened on the eastern slopes of theRocky Mountains allowing passage to the

south. By 10,000 years ago, western Canadawas ice-free but central and eastern Canadaremained covered by the Laurentide icesheet and large proglacial lakes (Fig. 7).Passage to eastern Canada north of theGreat Lakes was impossible at this time andthe only dispersal corridor was south of thelakes. By 8,400 years ago, moose arrivingin the eastern continent could have dis-persed westward north of the lakes, skirtingthe southern shores of the proglacial lakesto the north, and come into secondary con-tact with moose from the west once theproglacial lakes receded. Moose in theeastern part of the continent (A. a.americana) would have been on the end ofa series of founder events, explaining theirlow mitochondrial variability and the pres-ence of a contact zone between A. a.americana and the much more variable A.a. andersoni in Ontario between the GreatLakes and Hudson Bay.

Morphological AdaptationMoose of the Pleistocene and those that

entered North America at the beginning ofthe Holocene were significantly larger thanthose living today, a trait shared with othernorthern ruminants (Guthrie 1984). Guthrie(1984) proposed that the reduction in bodysize was an adaptation to changes in sea-sonal forage availability that occurred as aresult of climate amelioration at the end ofthe last ice age. The ability of moose torespond to a rapidly changing environmentbelies the relatively low levels of geneticvariation documented by the studies wehave reviewed and demonstrates that evo-lutionary potential is not easily predictedsolely by genetic variability but ultimately isdetermined by the presence of adaptivegenetic variation and heritability of traitsthat improve fitness (Lynch 1996).

A general reduction in body size is notthe only change to occur since the coloniza-tion of North America. Moose in


114

Fig. 7. Coverage of North America by theCordilleran and Laurentide ice sheets andproglacial lakes at 14,000, 10,000, and 8,400years ago (adapted from Dyke and Prest 1987).

North America exhibit many differences inbehavior and morphology. Alaskan mooseare perhaps the most divergent; they exhibita degree of sociality not observed else-where (Molvar and Bowyer 1994) and havemore distinctive body markings, also indica-tive of increased sociality (Bowyer et al.1991). Molvar and Bowyer (1994) sug-gested that moose in Alaska have evolvedsociality recently as a response to living inopen environments. Adaptation to openenvironments also applies to their matingsystem, which is harem-based. Haremmating is adaptive in open environments(Hirth 1977) where a male can protect a

harem from competitors. Moose elsewherein North America exhibit a tending-bondsystem of mating, which is adaptive forforested environments.

Moose in Alaska and Siberia exhibit thelargest body size of moose in North Americaand Eurasia, respectively. The similar ap-pearance of moose occurring on either sideof the Bering Strait has caused some inves-tigators to consider them the same subspe-cies (e.g., Telfer 1984). As moose fromthose 2 regions are not closely related(Hundertmark et al. 2002a,b), their similar-ity in size must result from convergent evo-lution. Both subspecies have adapted toopen, northern habitats by increasing bodysize. Adaptation to open habitats was dem-onstrated with a multivariate analysis ofantler size among moose inhabiting differ-ent areas and habitats in Alaska (Bowyer etal. 2002). Those moose inhabiting openhabitats (tundra) tended to have larger ant-lers overall than those living in boreal forest(taiga). Similarly, moose occupying moun-tainous habitat in the southern portions oftheir range in North America (A. a. shirasi)and Asia (A. a. cameloides) are similar;exhibiting small body and antler size (Geist1998). Bubenik (1998) explained that simi-larity by proposing a second entry into NorthAmerica by Asian moose—an entry thatbypassed Beringia by traveling along thesouthern coast of Alaska. Neither geneticnor fossil data support that hypothesis(Guthrie 1990, Hundertmark et al. 2002a,b,2003).

GENETIC EFFECTS OFMANAGEMENT

To this point we have discussed distri-bution of genetic and morphological diver-sity over space and time in the context ofgenetic drift and selection for locally adap-tive traits. Those patterns are developedover relatively long periods of time and areintegral to the process of evolution. Genetic


115

change also can occur over short periodsdue to human influences, notably harvestmanagement, and those changes may haveunintended and undesirable consequenceson individuals and populations (Harris et al.2002) and therefore are important to recog-nize.

Although it might be assumed that awell-designed harvest plan acts in a randomfashion on genetic makeup of individuals, inreality even a managed harvest can be ahighly selective force with measurable con-sequences in just a few generations(Coltman et al. 2003). Ryman et al. (1981)modeled the effect of different harvest strat-egies on 2 factors critical in determining theextent of genetic drift and inbreeding inpopulations: effective population size andgeneration interval, respectively. Hunt-ing strategies were defined by differentprobabilities of harvest for both juvenilesand adult females, and resulted in stablepopulations with decreased generation in-tervals and effective sizes compared withunhunted populations. Moreover, temporalchanges in genetic diversity differed fordifferent harvest strategies but always de-creased. Thus, Ryman et al. (1981) demon-strated that improperly designed harvestregimes can affect genetic characteristicsof populations and by extension may havean influence on evolutionary potential. Con-versely, Cronin et al. (2001) detected nodifferences in numbers of alleles or levelsof heterozygosity for 5 microsatellite lociamong 3 moose populations in Quebec, 1heavily hunted, 1 lightly hunted, and 1 nothunted.

Another critical factor in managementis the effect of harvest on genetic lociunderlying characters having a direct effecton reproductive fitness, e.g., antler size inmoose. Controlling harvest by defininglegal males according to antler size is com-mon in management of North American elk(Thelen 1991) and is a strategy employed in

moose management in British Columbia,Canada, and Alaska, USA (Child 1983,Schwartz et al. 1992). In an effort toevaluate genetic effects of the selectiveharvest system in Alaska, Hundertmark etal. (1993, 1998) modeled moose populationssubject to harvest strategies employing dif-ferent definitions of legal males. Theyconcluded that selective harvest systemscould result in allele frequency changes atloci coding for antler characteristics(Hundertmark et al. 1993) and that theposition of a population relative to nutri-tional carrying capacity of the habitat af-fected the rate of change in allele frequen-cies (Hundertmark et al. 1998). Thoseresults indicated that limiting harvest tomoose with large antlers could cause agenetically based decrease in antler sizeover time. Such a reduction in adaptivegenetic variation runs counter to generalconservation goals (Lynch 1996). A stun-ning example of the effect of harvest onfitness traits was recently reported byColtman et al. (2003), who documentedsignificant genetic effects on horn size andbody mass in bighorn sheep (Oviscanadensis) as a result of selective harvestof males with large horns.

Detecting potential changes in geneticcomposition of moose as they respond tovarious anthropogenic influences, whetherrelated to management or to changes in theenvironment, is a difficult task. Nonethe-less, it is an important area of investigationand deserves attention. Modeling exercisesand studies of genetic variation have notaddressed interrelationships of moosepopulations at fine scales. The effects ofmanagement and habitat alteration on proc-esses involved in maintenance of connec-tivity of moose populations, such as male-mediated gene flow via yearling dispersalare extremely important and should be de-scribed. Moose are highly adaptable ani-mals, but the intensive management of moose


116

populations and the environmental factorsinfluencing their habitat (e.g., wildfire) mayhave unintended and significant conse-quences on the moose genome through achange in selective forces. Proper conser-vation of this species requires that we rec-ognize and avoid that possibility.

ACKNOWLEDGEMENTSWe thank the organizers of the 5th Inter-

national Moose Symposium for the opportu-nity to synthesize and present this informa-tion. We wish to acknowledge funding sup-port from Federal Aid in Wildlife Restora-tion through the Alaska Department of Fishand Game as well as the Institute of ArcticBiology, University of Alaska Fairbanks. S.Côté and an anonymous reviewer providedconstructive comments for improving themanuscript.

REFERENCESANDERSON, P. M., A. V. LOZHKIN, and L. B.

BRUBAKER. 2002. Implications of a24,000-yr palynological record for aYounger Dryas cooling and for borealforest development in northeastern Si-beria. Quaternary Research 57:325-333.

ARKHIPOV, S. A., V. G. BESPALY, M. A.FAUSTOVA, O. Y. GLUSHKOVA, L. L.ISAEVA, and A. A. VELICHKO. 1986. Icesheet reconstructions. Pages 269-292in V. Šibrava, D. Q. Bowen, and G. M.Richmond, editors. QuaternaryGlaciations in the Northern Hemisphere.Pergamon Press, Oxford, U.K.

AVISE, J. C. 2000. Phylogeography: theHistory and Formation of Species.Harvard University Press, Cambridge,Massachusetts, USA.

_____, J. ARNOLD, R. M. BALL, JR., E.BERMINGHAM, T. LAMB, J. E. NEIGEL, C.A. REEB, and N. C. SAUNDERS. 1987.Intraspecific phylogeography: the mito-chondrial DNA bridge between popula-

tion genetics and systematics. AnnualReview of Ecology and Systematics18:489-522.

BIRKY, C. W., T. MARUYAMA, and P. FUERST.1983. An approach to population andevolutionary genetic theory for genes inmitochondria and chloroplasts, and someresults. Genetics 103:513-527.

BLUNDELL, G. M., M. BEN-DAVID, P. GROVES,R. T. BOWYER, and E. GEFFEN. 2002.Characteristics of sex-biased dispersaland gene flow in coastal river otters:implications for natural recolonizationof extirpated populations. MolecularEcology 11:289-303.

BOESKOROV, G. G. 1996. Karyotype ofmoose (Alces alces L.) from north-eastern Asia. Proceedings of the Rus-sian Academy of Sciences 329:506-508. (In Russian).

_____. 1997. Chromosomal differences inmoose. Genetika 33:974-978. (In Rus-sian).

BOWYER, R. T., D. M. LESLIE, JR., and J. L.RACHLOW. 2000. Dall’s and Stone’ssheep. Pages 491-516 in S. Demaraisand P. R. Krausman, editors. Ecologyand Management of Large Mammals inNorth America. Prentice Hall, UpperSaddle River, New Jersey, USA.

_____, J. L. RACHLOW, V. VAN

BALLENBERGHE, and R. D. GUTHRIE. 1991.Evolution of a rump patch in moose: anhypothesis. Alces 27:12-23.

_____, K. M. STEWART, B. M. PIERCE, K. J.HUNDERTMARK, and W. C. GASAWAY.2002. Geographical variation in antlermorphology of Alaskan moose: puta-tive effects of habitat and genetics.Alces 38: 155-165.

_____, V. VAN BALLENBERGHE, and J.G.KIE. 2003. Moose (Alces alces). Pages931 - 964 in G.A. Feldhamer, B.Thompson, and J. Chapman, editors.Wild Mammals of North America: Biol-ogy, Management, and Economics. Sec-


117

ond edition. The Johns Hopkins Uni-versity Press, Baltimore, Maryland,USA.

BRAEND, M. 1962. Studies on blood andserum groups in the elk (Alces alces).New York Academy of Sciences 97:296-305.

BRODERS, H. G., S. P. MAHONEY, W. A.MONTEVECCHI, and W. S. DAVIDSON.1999. Population genetic structure andthe effect of founder events on thegenetic variability of moose, Alcesalces, in Canada. Molecular Ecology8:1309-1315.

BRUFORD, M. W., D. J. CHEESMAN, T. COOTE,H. A. A. GREEN, S. A. HAINES, C.O’RYAN, and T. R. WILLIAMS. 1996.Microsatellites and their application toconservation genetics. Pages 278-297in T. B. Smith and R. K. Wayne, edi-tors. Molecular Genetic Approaches inConservation. Oxford University Press,Oxford, U.K.

BRUMFIELD, R. T., P. BEERLI, D. A.NICKERSON, and S. V. EDWARDS. 2003.The utili ty of single nucleotidepolymorphisms in inferences of popula-tion history. Trends in Ecology andEvolution 18:249-256.

BUBENIK, A. B. 1998. Evolution, taxonomyand morphophysiology. Pages 77-123in A. W. Franzmann and C. C. Schwartz,editors. Ecology and Management ofthe North American Moose.Smithsonian Institution Press, Wash-ington, D.C., USA.

CHESSER, R. K., C. REUTERWALL, and N.RYMAN. 1982. Genetic differentiationof Scandinavian moose Alces alcespopulations over short geographic dis-tances. Oikos 39:125-130.

CHILD, K. N. 1983. Selective harvest ofmoose in the Omineca: some prelimi-nary results. Alces 19:162-177.

COADY, J. W. 1982. Moose. Pages 902-922in J. A. Chapman and G. A. Feldhamer,

editors. Wild Mammals of NorthAmerica: Biology, Management, andEconomics. Johns Hopkins UniversityPress, Baltimore, Maryland, USA.

COLTMAN, D. W., P. O’DONOGHUE, J. T.JORGENSON, J. T. HOGG, C. STROBECK,and M. FESTA-BIANCHET. 2003. Unde-sirable evolutionary consequences oftrophy hunting. Nature 426:655-658.

CRONIN, M. A. 1992. Intraspecific variationin mitochondrial DNA of North Ameri-can cervids. Journal of Mammalogy73:70-82.

_____, J. C. PATTON, R. COURTOIS, and M.CRÊTE. 2001. Genetic variation ofmicrosatellite DNA in moose in Québec.Alces 37:175-187.

DYKE, A. S., and V. K. PREST. 1987. LateWisconsinan and Holocene history ofthe Laurentide ice sheet. GeographiePhysique et Quaternaire 41:237-263.

ELIAS, S. A. 2000. Late Pleistocene cli-mates of Beringia, based on analysis offossil beetles. Quaternary Research53:229-235.

ELLEGREN, H., L. ANDERSSON, and K. WALLIN.1991. DNA polymorphism in moose(Alces alces) revealed by polynucle-otide probe (TC)n. Journal of Heredity82:429-431.

_____, S. MIKKO, K. WALLIN, and L.ANDERSSON. 1996. Limited polymor-phism at major histocompatibility com-plex (MHC) loci in the Swedish mooseA. alces. Molecular Ecology 5:3-9.

FLEROV, K. K. 1952. Fauna of the USSR:Mammals. Vol. 1 no 2. Musk deer anddeer. The Academy of Sciences of theUSSR, Leningrad. (English translationby the Israel Program for ScientificTranslation, 1960, S. Monson, Jerusa-lem).

FRANZMANN, A. W., and C. C. SCHWARTZ,editors. 1998. Ecology and Manage-ment of the North American Moose.Smithsonian Institution Press, Wash-


118

ington, D.C., USA.FRIES, R., and G. DURSTEWITZ. 2001.

DigitalDNA signatures: SNPs for ani-mal tagging. Nature Biotechnology19:508.

FULTON, R. J., M. M. FENTON, and N. W.RUTTER. 1986. Summary of Quater-nary stratigraphy and history, westernCanada. Pages 229-242 in V. Šibrava,D. Q. Bowen, and G. M. Richmond,editors. Quaternary Glaciations in theNorthern Hemisphere. Pergamon Press,Oxford, U.K.

GEIST, V. 1987a. On the evolution andadaptations of Alces. Swedish WildlifeResearch Supplement 1:11-23.

_____. 1987b. On speciation in Ice Agemammals, with special reference tocervids and caprids. Canadian Journalof Zoology 65:1067-1084.

_____. 1998. Deer of the World: TheirEvolution, Behavior, and Ecology.Stackpole Books, Mechanicsburg, Penn-sylvania, USA.

GROVES, C. P., and P. GRUBB. 1987. Rela-tionships of living deer. Pages 3-59 inC. M. Wemmer, editor. Biology andManagement of the Cervidae.Smithsonian Institution Press, Wash-ington, D.C., USA.

GUTHRIE, R. D. 1984. Alaska megabucks,megabulls, and megarams: the issue ofPleistocene gigantism. Special Publi-cations of the Carnegie Museum ofNatural History 8:482-509.

_____. 1990. New dates in AlaskanQuaternary moose, Cervalces-Alces –archaeological, evolutionary and eco-logical implications. Current Researchin the Pleistocene 7:111-112.

_____. 1995. Mammalian evolution inresponse to the Pleistocene-Holocenetransition and the break-up of the mam-moth steppe: two case studies. ActaZoologica Cracoviensia 38:139-154.

GYLLENSTEN, U., C. REUTERWALL, N. RYMAN,

and G. STAHL. 1980. Geographicalvariation in transferrin allele frequen-cies in three deer species from Scandi-navia. Hereditas 92:237-241.

HANCOCK, J. M. 1999. Microsatellites andother simple sequences: genomic con-text and mutational mechanisms. Pages1-9 in D. B. Goldstin and C. Schlötterer,editors. Microsatellites: Evolution andApplications. Oxford University Press,Oxford, U.K.

HARRINGTON, R. 1985. Evolution and distri-bution of the Cervidae. Biology of deerproduction. The Royal Society of NewZealand, Bulletin 22:3-11.

HARRIS, R. B., W. A. WALL, and F. W.ALLENDORF. 2002. Genetic conse-quences of hunting: what do we knowand what should we do? Wildlife Soci-ety Bulletin 30:634-643.

HEDRICK, P. W. 1994. Evolutionary genet-ics of the major histocompatibility com-plex. American Naturalist 143:945-964.

HEWITT, G. M. 1996. Some genetic conse-quences of ice ages, and their role indivergence and speciation. BiologicalJournal of the Linnaen Society 58:247-276.

HIRTH, D. H. 1977. Social behavior ofwhite-tailed deer in relation to habitat.Wildlife Monographs 53.

HUNDERTMARK, K. J., R. T. BOWYER, G. F.SHIELDS, and C. C. SCHWARTZ. 2003.Mitochondrial phylogeography of moose(Alces alces) in North America. Jour-nal of Mammalogy 84:718-728.

_____, P. E. JOHNS, and M. H. SMITH.1992. Genetic diversity of moose fromthe Kenai Peninsula, Alaska. Alces28:15-20.

_____, G. F. SHIELDS, R. T. BOWYER, and C.C. SCHWARTZ. 2002a. Genetic relation-ships deduced from cytochrome-b se-quences among moose. Alces 38:113-122.


119

_____, _____, I. G. UDINA, R. T. BOWYER,A. A. DANILKIN, and C. C. SCHWARTZ.2002b. Mitochondrial phylogeographyof moose (Alces alces): late Pleistocenedivergence and population expansion.Molecular Phylogenetics and Evolution22:375-387.

_____, T. H. THELEN, and R. T. BOWYER.1998. Effects of population density andselective harvest on antler phenotype insimulated moose populations. Alces34:375-383.

_____, _____, and C. C. SCHWARTZ. 1993.Genetic and population effects of se-lective harvest systems in moose: amodeling approach. Alces 29:225-234.

IRWIN, D. M., T. D. KOCHER, and A. C.WILSON. 1991. Evolution of the cyto-chrome b gene in mammals. Journal ofMolecular Evolution. 32: 128 - 144.

JOUZEL, J., C. LORIUS, J. R. PETIT, C. GENTHON,N. I. BARKOV, V. M. KOTLYAKOV, and V.M. PETROV. 1987. Vostok ice core: acontinuous isotope temperature recordover the last climate cycle (160,000years). Nature 329:403-408.

LISTER, A. M. 1993. Evolution of mam-moths and moose: the Holarctic per-spective. Pages 178-204 in A. D.Barnosky, editor. Quaternary Mam-mals of North America. CambridgeUniversity Press, Cambridge, U.K.

LOPEZ, J. V., M. CULVER, J. C. STEPHENS, W.E. JOHNSON, and S. J. O’BRIEN. 1997.Rates of nuclear and cytoplasmic mito-chondrial DNA sequence divergence inmammals. Molecular Biology and Evo-lution 14:277-286.

LYNCH, M. 1996. A quantitative-geneticperspective on conservation issues.Pages 471-501 in J. C. Avise and J. L.Hamrick, editors. Conservation Genet-ics: Case Studies from Nature.Chapman & Hall, New York, NewYork, USA.

MASON, O. K., P. M. BOWERS, and D. M.

HOPKINS. 2001. The early Milankovitchthermal maximum and humans: ad-verse conditions for the Denali complexof eastern Beringia. Quaternary Sci-ence Reviews 20:525-548.

MIKKO, S., and L. ANDERSSON. 1995. Lowmajor histocompatibility complex classII diversity in European and NorthAmerican moose. Proceedings of theNational Academy of Sciences, USA92:4259-4263.

MIYAMOTO, M. M., F. KRAUS, and O. A.RYDER. 1990. Phylogeny and evolutionof antlered deer determined from mito-chondrial DNA sequences. Proceed-ings of the National Academy of Sci-ences, USA 87:6127-6131.

MOLVAR, E. M., and R. T. BOWYER. 1994.Costs and benefits of group living in arecently social ungulate: the Alaskanmoose. Journal of Mammalogy 75:621-630.

MULLIS, K., F. FALOONA, S. SCHARF, R. SAKAI,G. HORN, and H. ERLICH. 1986. Specificenzymatic amplification of DNA in vitro:the polymerase chain reaction. ColdSpring Harbor Symposia in Quantita-tive Biology 51:263-273.

NADLER, C. F., C. E. HUGHES, K. E. HARRIS,and N. W. ADLER. 1967. Electrophore-sis of the serum proteins and transferrinsof Alces alces (elk), Rangifer tarandus(reindeer), and Ovis dalli (Dall sheep)from North America. ComparativeBiochemistry and Physiology 23:149-157.

NEVO, E. 1978. Genetic variation in naturalpopulations: patterns and theory. Theo-retical Population Biology 13:121-177.

PETERSON, R. L. 1955. North AmericanMoose. University of Toronto Press,Toronto, Ontario, Canada.

QUELLAR, D. C., J. E. STRASSMANN, and C.R. HUGHES. 1993. Microsatellites andkinship. Trends in Ecology and Evolu-tion 8:285-288.


120

RØED, K. H., and L. MIDTHJELL. 1998.Microsatellites in reindeer, Rangifertarandus, and their use in other cervids.Molecular Ecology 7:1773-1776.

RYMAN, N., R. BACCUS, C. REUTERWALL, andM. H. SMITH. 1981. Effective popula-tion size, generation interval, and poten-tial loss of genetic variability in gamespecies under different hunting regimes.Oikos 36:257-266.

_____, G. BECKMAN, G. BRUUN-PETERSEN,and C. REUTERWALL. 1977. Variabilityof red cell enzymes and genetic implica-tions of management policies inScandinavian moose (Alces alces).Hereditas 85:157-162.

_____, C. REUTERWALL, K. NYGREN, and T.NYGREN. 1980. Genetic variation anddifferentiation in Scandinavian moose(Alces alces): are large mammalsmonomorphic. Evolution 34:1037-1049.

SAGE, R. D., and J. O. WOLFF. 1986.Pleistocene glaciations, fluctuatingranges, and low genetic variability in alarge mammal (Ovis dalli). Evolution40: 1092 - 1095.

SCHWARTZ, C. C., K. J. HUNDERTMARK, andT. H. SPRAKER. 1992. An evaluation ofselective bull moose harvest on the KenaiPeninsula, Alaska. Alces 28:1-13.

SCRIBNER, K. T., and R. K. CHESSER. 2001.Group-structured genetic models inanalysis of the population and behavioralecology of poikilothermic vertebrates.Journal of Heredity 92:180-189.

SELANDER, R. K., and D. W. KAUFMAN.1973. Genic variability and strategiesof adaptation in animals. Proceedingsof the National Academy of Sciencesof the USA 70:1875-1877.

SHER, A. V. 1987. History and evolution ofmoose. Swedish Wildlife ResearchSupplement 1:71-97.

SHUBIN, P. N. 1969. The genetics oftransferrins in the reindeer and in theEuropean elk. Genetika 5:37-41. (In

Russian).SMITH, M. H., R. BACCUS, H. O. HILLESTAD,

and M. N. MANLOVE. 1984. Populationgenetics. Pages 119-128 in L. K. Halls,editor. White-tailed Deer: Ecology andManagement. Stackpole Books,Harrisburg, Pennsylvania, USA.

_____, K. T. SCRIBNER, L. H. CARPENTER,and R. H. GARROTT. 1990. Genetic char-acteristics of Colorado mule deer(Odocoileus hemionus) and compari-sons with other cervids. SouthwesternNaturalist 35: 1 - 8.

SYMONDSON, W. O. 2002. Molecular iden-tification of prey in predator diets.Molecular Ecology 11:627-641.

TELFER, E. S. 1984. Circumpolar distribu-tion and habitat requirements of moose(Alces alces). Pages 145-182 in R.Olson, F. Geddes, and R. Hastings, edi-tors. Northern Ecology and ResourceManagement. University of AlbertaPress, Edmonton, Canada.

THELEN, T. H. 1991. Effects of harvest onantlers of simulated populations of elk.Journal of Wildlife Management 55:243-249.

THOUVENY, N., and E. BONIFAY. 1984. Newchronological data on EuropeanPlio-Pleistocene faunas and hominidoccupation sites. Nature 308:355-358.

UDINA, I. G., A. A. DANILKIN, and G. G.BOESKOROV. 2002. Genetic diversity ofmoose (Alces alces L.) in Eurasia.Genetika 38:951-957. (In Russian).

VERNESI, C., E. PECCHIOLO, D. CARAMELLI, R.TIEDEMANN, E. RANDI, and G. BERTORELLE.2002. The genetic structure of naturaland reintroduced roe deer (Capreoluscapreolus) populations in the Alps andcentral Italy, with reference to the mito-chondrial DNA phylogeography of Eu-rope. Molecular Ecology 11:1285-1297.

WILHELMSON, M., R. K. JUNEJA, and S.BENGTSSON. 1978. Lack of polymor-phism in certain blood proteins and en-


121

zymes of European and Canadianmoose. Naturaliste Canadien 105:445-449.

WILSON, G. A., C. STROBECK, L. WU, and J.W. COFFIN. 1997. Characterization ofmicrosatellite loci in caribou Rangifertarandus, and their use in otherartiodactyls. Molecular Ecology 6:697-699.

WILSON, P. J., S. GREWAL, A. RODGERS, R.REMPEL, J. SAQUET, H. HRISTIENKO, F.BURROWS, R. PETERSON, and B. N.WHITE. 2003. Genetic variation andpopulation structure of moose (Alcesalces) at neutral and functional DNAloci. Canadian Journal of Zoology81:670-683.

ZHELEZNOV, N. K. 1993. Historic andcurrent distribution of moose in thenortheast USSR. Alces 29:213-218.


122

Term Definition

Adaptive genetic variation Genotypic variation at loci that control traits important to fitness, such as morphology, physiology, and behavior.

Allozyme A gene product (protein) that is distinguished by its migratory characteristics in a gel exposed to an electric field (electrophoresis). Differences among alleles (different variants of the same gene) at allozyme loci relate to amino acid composition and secondary structure of the protein. Only mutations that create proteins with different migratory characteristics are detectable.

Control region A portion of mtDNA that evolves (incorporates mutations) at a very fast rate, which makes it a valuable marker for examining intraspecific genetic variation. Occasionally referred to as the D-loop.

DNA sequence The ultimate level of analysis of genetic material. This technique deduces the identity and order of nucleotides in a fragment of DNA. Mutations (nucleotide substitutions) are detectable whether or not they create different gene products.

Effective population size The size of a standardized population that has the same degree of genetic drift as the population being studied. An ideal population is a closed population of constant size with non-overlapping generations and no variance in reproductive success. The smaller the effective size of a population, the faster it will lose genetic diversity through drift regardless of actual population size. Effective population size (Ne) is almost always a fraction of the true population size (N).

Generation interval Mean age of all parents.

Genetic drift Changes in allele frequencies across generations due to random sampling error associated with less than infinite population size.

Haplotype The haploid equivalent of genotype. Genetic type of an individual when haploid DNA, such as mtDNA, is analyzed.

Heritability The proportion of variance in the expression of a trait, such as antler size or body size, that is due to genetic effects (as opposed to environmental effects), i.e., the degree to which a trait can be passed on to the next generation.

Microsatellite Segments of DNA composed of sequence units varying from 2-4 nucleotides in length that are tandemly repeated. Size variation (number of repeated units) defines alleles. Microsatellites are Mendelian in their inheritance, i.e., they are diploid, specific to a site on a chromosome, and occur in either a homozygous or heterozygous genotype.

Minisatellite Similar to microsatellites except that the repeat units vary from 16-64 nucleotides in length and occur at many sites throughout the chromosomes, thus exhibiting more than 2 alleles per individual and creating complex genotypes of gel banding patterns that resemble bar codes. This is the technique that pioneered genetic fingerprinting.

Mitochondrial DNA (mtDNA) A circular DNA molecule occurring in the mitochondrion. Unlike chromosomes, which occur in pairs (diploid), mtDNA occurs as a single copy (haploid) because it is inherited only from the maternal line. Therefore, it is not subject to recombination and changes only via mutation. That property makes it particularly useful for tracing lineages through time.

Molecular clock The assumption that the average rate of mutation for a particular DNA sequence is constant over evolutionary time. If a molecular clock can be assumed, the amount of genetic divergence between populations or species can be converted to time since divergence.

Phylogeography The study of genetic lineages in a spatial and temporal context, revealing historic population processes and evolutionary histories.

RFLP Restriction Fragment Length Polymorphism – a section of DNA of known length is digested with restriction enzymes (endonucleases), which cleave DNA at sites with specific target sequences of 4-6 nucleotides. The digested fragments are separated by length (number of nucleotides) using gel electrophoresis and haplotypes are characterized by numbers and sizes of fragments.

Appendix 1. Glossary of specialized terms used in this review.

genetics, evolution, and phylogeography of...

Documents