4013.p65 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, genetic heterogeneity of moose is relatively low compared with other mammals. Similarly, variation in mitochondrial DNA of moose is limited worldwide, indicating low historic effective population size and a common ancestry for moose within the last 60,000 years. That ancestor most likely lived in central Asia. Moose likely exhibit low levels of heterogeneity because of population bottlenecks in the late Pleistocene caused by latitudinal shifts in habitat from recurrent climate reversals. A northward movement of boreal forest associated with the end of the last ice age facilitated the northward advance of Asian populations and colonization of the New World, which occurred as a 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 ability to adapt to a changing environment, indicating that limited neutral genetic variation may not indicate limited adaptive genetic variation. We conclude that morphological variation among moose worldwide occurred within a few thousand years and indicates that moose underwent episodes of rapid and occasionally convergent evolution. Genetic change in moose populations over very short time scales (tens or hundreds of years) is possible under harvest management regimes and those changes may not be beneficial to moose in the long term. Modeling exercises have demonstrated that harvest strategies can have negative consequences on neutral genetic variation as well as alleles underpinning fitness traits. Biologists should consider such outcomes when evaluating management 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 in biological investigations, and provide ana- lytical tools that are applicable across a broad spectrum of investigation. For in- stance, genetic analysis can provide insights into such diverse investigations as evolu- tionary histories of species (Avise et al. 1987, 2000), interactions and relationships among populations (Blundell et al. 2002) or individuals (Quellar et al. 1993), evaluation of the success of specific management ac- tions (Vernesi et al. 2002), population and behavioral ecology (Scribner and Chesser 2001), and food habits (Symondson 2002). Recent advances in collection and analysis of genetic data have facilitated more re- fined approaches to evolutionary and popu- lation genetic questions, and our under- standing of moose biology has benefited as a result of those advances. Evolution and taxonomy of moose (Alces alces) 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 of behavior, morphology, paleontology, and genetics, but no review has dealt specifi- HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 104 cally with genetics. In this review, our goal is to provide an overview of older studies while focusing on recent advances in genet- ics and phylogeography (see definition in Appendix 1) of moose and the insights they provide. The broad scope of genetic and evolu- tionary investigations in species biology would make a complete review of all studies disjointed. Yet, approximately half of all published studies of moose genetics have been published since the comprehensive treatise “Ecology and Management of the North American Moose” (Franzmann and Schwartz 1998) was compiled; thus, we were compelled to present the most com- plete review possible. In an effort to present a 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 the conclusions drawn from those studies; (2) moose evolution and phylogeography, where we examine the evolutionary descent of moose and processes that have shaped the genetic variation and structure observed today; and (3) genetic effects of harvest, which reviews a small but important body of work composed of management-based modeling that examined effects of various harvest regimes on population and genetic measures. ASSESSING GENETIC DIVERSITY One potential difficulty in discussing genetic analyses is the use of specialized terminology. To avoid uncertainty and en- hance understanding, we provide a brief glossary of terms used in this review (Ap- pendix 1). Terms defined in the glossary are highlighted in bold in the text at their first usage. The Allozyme Era First reports of genetic investigations of moose were published by Braend (1962, cited by Gyllensten et al. 1980), Nadler et al. (1967), and Shubin (1969, cited by Gyllensten et al. 1980), wherein those au- thors examined electrophoretic variation in proteins from blood serum; no variation in those 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 of Sweden for polymorphism at 23 allozyme loci. That study reported only 1 locus to be polymorphic, however, and only in 1 region. Although they suspected that allele fre- quencies varied geographically within the 1 variable region, the difference was not sta- tistically significant. Those authors con- cluded that genetic drift associated with a severe population bottleneck (reduction in population size) in Sweden in the 19th cen- tury was a probable cause of the observed lack of diversity. Wilhelmson et al. (1978), examining variation in serum proteins, noted no differences between Canadian and Eu- ropean moose. From that evidence, they concluded that moose populations on sepa- rate continents had not undergone signifi- cant genetic drift despite being separated for thousands of years, implying that effec- tive population sizes of moose populations historically had been large. Wilhelmson et al. (1978) also proposed that historic population bottlenecks in Swe- den had not been severe enough to have had an effect on genetic diversity of moose. Gyllensten et al. (1980) conducted exten- sive screening of a transferrin locus from moose across Fennoscandia and detected a single polymorphism occurring in Norway, Sweden, and Finland. Nonetheless, the poly- morphism was present in only 6 of 16 populations and the uncommon allele never exceeded 6% in any population. The au- thors presented differences in frequency of the uncommon allele as evidence of differ- ALCES VOL. 40, 2004 MOOSE GENETICS - HUNDERTMARK AND BOWYER 105 entiation of populations geographically, sup- porting observations of Ryman et al. (1977). Reliance on the occurrence of a single rare polymorphism to demonstrate population subdivision, however, is tenuous at best. Those early studies and others created an impression among some biologists that certain species, including moose, possessed little genetic variation across the genome. Hypotheses explaining this in evolutionary terms were proposed. Selander and Kaufman (1973) proposed the environmen- tal-grain hypothesis, which stated that large, highly mobile animals exhibited less genetic variability than small, sedentary species. That hypothesis further stated that highly mobile mammals would exhibit greater ho- mogeneity across large areas than more sedentary forms. Other hypotheses pro- posed that r-strategists were less variable than K-strategists (Harrington 1985), ge- netic heterogeneity was greater in species inhabiting broad arrays of habitats com- pared with habitat specialists (Nevo 1978), or that northern cervids inhabiting boreal forests were less variable than their rela- tives to the south (Smith et al. 1990). Analyses of 23 allozyme loci in > 700 i n d i v i d u a l s r e p r e s e n t i n g 1 8 m o o s e populations in Scandinavia were required to reveal extensive genetic variation in moose (Ryman et al. 1980). Those authors refuted the environmental-grain hypothesis, con- cluding that large mammals in general, and large cervids in particular, are not naturally monomorphic; previous studies of moose had examined too few loci or individuals to detect variation. Nonetheless, those au- thors noted that genetic variability in moose was somewhat less than that observed in many other species of mammals (Nevo 1978), but that genetic drift due to small historic population size was a more likely explanation than any specific evolutionary strategy. Thus, genetic drift was once again proposed 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 a single 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 scales small enough to be considered within a single population illustrated that structure of moose populations existed at scales smaller than previously imagined, and that vagility was not inconsistent with genetic structur- ing. The most recent study of allozyme vari- ation in moose reported extensive variation i n a m o o s e p o p u l a t i o n i n A l a s k a (Hundertmark et al. 1992). The level of genetic diversity observed was greater than that reported elsewhere in moose and was similar to levels observed in white-tailed deer, a species known for extensive allozyme diversity (Smith et al. 1984). Hundertmark et al. (1992) hypothesized that lesser levels of variability described in moose from Scan- dinavia and other regions of North America were attributable to glacial history. All other moose populations studied to that point occurred in previously glaciated terrain that was colonized by moose after retreat of Pleistocene ice sheets. Colonization of previously glaciated areas could have re- sulted in serial founder events that reduced genetic diversity (Sage and Wolff 1986). Hundertmark et al. (1992) argued that Alaska could have served as a refugium for moose in which genetic diversity could have been maintained because of a large effec- tive population size. Assessing Variation at the Sequence L e v e l The first investigation of highly poly- morphic molecular markers in moose docu- mented 4 alleles in a microsatellite-like HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 106 locus in 17 individuals from Sweden (Ellegren et al. 1991). Eight genotypes were re- ported, which represented a heretofore un- thinkable level of polymorphism. Those authors investigated the inheritance of that locus in a 2-generation pedigree and deter- mined that the alleles exhibited Mendelian inheritance. That study and others like it laid the foundation for the explosion of i n t e r e s t i n p o p u l a t i o n g e n e t i c s a n d phylogenetics based on molecular markers and the polymerase chain reaction (PCR; Mullis et al. 1986). The advent of PCR represented one of the truly significant advances in the history of molecular biology and genetics. The process allows in-vitro amplification of DNA from miniscule amounts of starting material (theoretically as little as 1 molecule of DNA) to provide sufficient quantities for analysis. No longer were researchers required to sacrifice animals to acquire sufficient quan- tities and types of tissues for genetic analy- ses because any nucleated cell held the complete genetic complement of the indi- vidual. PCR offered unsurpassed access to the genome, and researchers soon applied that to study genetics of moose. Mikko and Andersson (1995) conducted the first analysis of functional loci in an analysis of variation in the major histocom- patibility complex (MHC) in moose from Sweden and Canada. The MHC is a family of genes important in immune system func- tion, and low levels of diversity of MHC alleles have been interpreted as indicators of lost evolutionary potential and increased susceptibility to pathogens (Hedrick 1994). Mikko and Andersson (1995) noted very low levels of MHC variation in both Swed- ish and Canadian moose. Moreover, those authors documented similarity among alleles between continents and inferred the exist- ence of a bottleneck in an ancient moose lineage prior to divergence of European and Canadian lineages. Mikko and Andersson (1995) applied a molecular clock to DNA sequence variation in the control region of mitochondrial DNA (mtDNA) to date the time of divergence of Swedish and Canadian moose, which they estimated at 165,000-350,000 years ago. The time since divergence of European moose also was analyzed by Ellegren et al. ( 1 9 9 6 ) . T h e y a s s e s s e d v a r i a t i o n i n minisatellite loci of Swedish moose and concluded that normal evolutionary proc- esses could have generated the amount of variation observed within 10,000-50,000 years after a severe bottleneck. Their implication, therefore, was that the estimate of divergence provided by Mikko and Andersson (1995) was too old by perhaps 1 order of magnitude. Surprisingly, the two data sets are not inconsistent; indeed, they show similar levels of variation considering differences in evolutionary rates among marker types. The differences in estimates for date of divergence relate more to the evolutionary rate estimates used than to differences in genetic variability. Microsatellite loci were first described for moose by Wilson et al. (1997) and Røed and Midthjell (1998). Broders et al. (1999) demonstrated the utility of microsatellites for assessing population structure in moose by assessing consequences of founder events in Canada. Heterozygosity in 3 populations founded by few individuals de- creased from 14-30% compared with the source population. Broders et al. (1999), in assessing variability of moose on the island of Newfoundland, Canada, demonstrated that 2 consecutive founder events reduced heterozygosity by 46%. Although they could not discern any decrease in fitness as a result of the decrease in diversity, the au- thors questioned the long-term viability of those moose populations. Nonetheless, lev- els of diversity in neutral microsatellite loci were not indicative of diversity in functional loci in moose (Wilson et al. 2003). ALCES VOL. 40, 2004 MOOSE GENETICS - HUNDERTMARK AND BOWYER 107 The Future Microsatellites have replaced allozymes as the most widely used molecular marker for assessing nuclear genetic diversity, and will be the choice of geneticists for the foreseeable future (Bruford et al. 1996). There are problems, however, with analysis of microsatellites because the ways in which they mutate into new forms are not entirely understood (Hancock 1999). In the future, a new type of analysis called single nucle- otide polymorphism (SNP, pronounced “snip”) may replace microsatellites for some applications (Fries and Durstewitz 2001, Brumfield et al. 2003). This new technol- ogy allows a single nucleotide site to be queried 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 “DNA chips”) allows for fast and accurate exami- nation of many individuals and SNPs, but we must await the development and char- acterization of marker loci before broad application of this new family of molecular markers can be considered. MOOSE EVOLUTION AND PHYLOGEOGRAPHY Origins of Modern Moose Moose (Alces alces) are a young spe- cies in the evolutionary scheme of large mammals. The genus Alces first appears in the fossil record 2 million years ago (Thouveny and Bonifay 1984) and fossils attributable to A. alces are first recorded approximately 100,000 years ago (Lister 1993). Those dates are very recent consid- ering that the subfamily Odocoileinae, to which moose belong, diverged from other deer lineages 9-12 million years ago (Miyamoto et al. 1990). Paleontological evidence indicated Eu- rope as the place of origin of the genus Alces (Lister 1993). The genus never was diverse, with only one species present in the fossil record at any particular time. Yet, the species assumed to be the precursor to A. a l c e s , t h e b r o a d - f r o n t e d m o o s e ( A . latifrons) was distributed across Eurasia and into northwestern North America for a time before becoming extinct in Beringia at the end of the Pleistocene (Guthrie 1995). Thus, the widespread distribution of modern moose and its immediate ancestor indicate a degree of evolutionary success despite a paucity of species diversity. Up to 8 subspecies of moose are recog- nized worldwide (Fig. 1); 4 in Eurasia and 4 in North America (Peterson 1955). That number is open to question, however. Geist (1987a, 1998) contends that there are 2 predominant types of moose in the world: American and European, following the con- vention of Flerov (1952). To the former type he assigns all North American moose as well as eastern Asian subspecies A. a. burturlini and A. a. pfizenmayeri. He based his opinion primarily on morphology and noted similar geographic divisions in taxonomy among reindeer and caribou (Rangifer tarandus) and red deer and North American 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 North America. He also suggested that A. a. a m e r i c a n u s h a s p r e c e d e n c e u n d e r nomenclatural conventions as the proper name for the east Asian-North American s u b s p e c i e s . H e r e f e r r e d t o 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 to some degree by karyotype (Boeskorov 1996, 1997) and some data on mtDNA (Mikko HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 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 population in Newfoundland. and Andersson 1995). Most Eurasian moose have a karyotype of 2N = 68, whereas North American moose have 2N = 70. That difference derives from a Robertsonian translocation of 2 acrocentric chromosomes into a single metacentric chromosome or vice versa. Although that chromosomal polymorphism originally was thought to sepa- rate Eurasian and North American moose (Groves and Grubb 1987), the 2N = 70 form was recently discovered in eastern Asia (Boeskorov 1996, 1997). Similarly, a length mutation (insertion-deletion, or indel) within the control region of mtDNA originally was described as discriminating between North American and European moose (Mikko and Andersson 1995), but subsequent investiga- tions documented that indel in moose from Eastern Asia (Hundertmark et al. 2002b, Udina et al. 2002). Although the precise g e o g r a p h i c d i s t r i b u t i o n s o f t h o s e polymorphisms in karyotype and mtDNA ALCES VOL. 40, 2004 MOOSE GENETICS - HUNDERTMARK AND BOWYER 109 length are not well described, they seem to correspond geographically with a zone of intergradation in east-central Asia, similar to that proposed for American and Eurasian types of moose (Flerov 1952, Geist 1998). More work is needed to determine the ex- tent of that geographic correspondence and to determine if it coincides with subspecies boundaries. Moreover, the question of re- productive viability of the two chromosomal races must be addressed. Indeed, Boeskorov (1997) has proposed that the chromosomal races are different species and Groves and Grubb (1987) have identified them as “semi- species.” We caution, however, that chro- mosome numbers may be a poor designator of species among large mammals (Bowyer et al. 2000). Hundertmark et al. (2002b) tested the 2-types hypothesis by examining the distri- bution of genetic variance of mtDNA among and within different hypothetical population structures. Those authors sampled moose throughout their worldwide distribution and arranged them into either 2 groups (corre- sponding to the 2-types hypothesis) or 3 groups corresponding to continent of origin (Asia, Europe, and North America). They then examined the distribution of genetic variance within and among or between groups, predicting that the correct structure would minimize within-group variation and maximize among-group variation. Percent- age of total variation observed among the 3 groups was slightly greater than variation between the 2 groups (61.5% vs. 58.1%), and variation among populations within groups was minimized in the 3-group com- parison (21.6% vs. 28.8% in the 2-group comparison). Therefore, Hundertmark et al. (2002b) concluded that mtDNA data provided no support for a 2-type over a 3- type hypothesis. That finding can be visu- alized by a phylogenetic tree constructed from haplotypes originally reported by Hundertmark et al. (2002b, 2003), which shows North American moose as distinct from both Asian and European forms (Fig. 2). Ancient Bottlenecks and the Mother of All 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 constructing mammalian phylogenies (Irwin et al. 1991) and a paucity of variation in moose indi- cated a recent common ancestry likely due to a severe bottleneck that affected all extant lineages (Hundertmark et al. 2002a), which is in agreement with the findings of Mikko and Andersson (1995). Analysis of variation within the mitochondrial control region, which evolves at a much faster rate than cytochrome b (Lopez et al. 1997), was Fig. 2. Unrooted phylogenetic tree of moose populations and subspecies worldwide, with the exception of A. a. pfizenmayeri, using FST a s t h e d i s t a n c e m e a s u r e [ d a t a f r o m Hundertmark et al. (2002b, 2003)]. Note the distinct positions of the 3 Eurasian subspe- cies and North American moose, which do not support an hypothesis of 2 or 3 races of moose worldwide. HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 110 Fig. 3. A phylogenetic tree of haplotypes of the mitochondrial control region of moose. Sym- bols indicate region of origin, with black sym- bols indicating Asian origin. Distinct clades or phylogroups are indicated on the right. From Hundertmark et al. (2002b). necessary to reveal significant levels of variation in moose and subsequently geo- graphic patterns were revealed. Control region haplotypes of moose can be divided into 3 clades, or haplogroups (Fig. 3). The basal haplogroup (i.e., the group that diverges first from the base of the tree) is entirely Asian, which suggests that those are the oldest moose haplotypes. The two other haplogroups are primarily European and primarily North American, although some Asian haplotypes occur in both. The distribution of haplogroups on a worldwide scale illustrates the age of con- tinental assemblages of haplotypes (Fig. 4). The Yakutia area contains moose from all 3 haplogroups. The Russian Far East con- tains both European and Asian haplogroups, but not North American, and both Europe a n d N o r t h A m e r i c a c o n t a i n o n l y 1 haplogroup each. Therefore, Yakutia can be identified as the area from which all extant moose lineages were derived, i.e., it is the oldest extant moose population that has been sampled. Yakutia probably was the center of a single moose population during the last ice age, or at least was the location of the only population to provide descendants of mod- ern moose. Moose would have been re- stricted in their distribution because the cooler climate in Asia at that time would have resulted in a shift of boreal forest habitat to the south. That habitat could have shifted only so far southward, because of prominent mountains running east-west, which would have formed an effective bar- rier to further movement to the south (Hewitt 1996). During the last ice age, there were 2 periods of maximum glacial advance, termed the lower and upper pleniglacials. Those episodes occurred at approximately 62,000 and 20,000 years ago, respectively (Fulton et al. 1986). Boreal forest habitats in Asia would have shifted to the south during those cooling episodes and would have been com- pressed against the northern slopes of moun- Fig. 4. Distribution of mitochondrial haplogroups worldwide. Note that moose from the Yakutia area have the most diverse composition and that moose from North America do not share haplogroups with moose from Russian Far East. ALCES VOL. 40, 2004 MOOSE GENETICS - HUNDERTMARK AND BOWYER 111 59,000 and 14,000 years ago. When expan- sion times of moose are overlaid on a profile of global temperature change for the last ice age (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 with the late Pleistocene and early Holocene. Coming to America Cronin (1992) analyzed subspecific vari- ation in North American cervids using re- striction fragment length polymorphisms (RFLP) of mtDNA. Despite analyzing 32 moose sampled from different regions of North America, he documented no varia- tion among haplotypes from that continent. In comparison to other North American cervids, the lack of variation among subspe- cies of moose was interpreted as an indica- Fig. 5. Glacial coverage during the last glacial maximum, superimposed on a map of present- day sea level. Note that the Bering land bridge between North America and Asia would have been exposed during the glacial maximum due to lower sea levels. Names of major ice sheets are provided. tain ranges. During subsequent warming intervals, moose habitat would have spread to the north, allowing moose populations to expand (Guthrie 1995). Unlike North America, much of Eurasia was not glaci- ated during those periods (Arkhipov et al. 1986), providing potential dispersal routes across the continent (Fig. 5). The process of latitudinal shifts of range associated with episodes of climate change results in de- creases of existing genetic diversity (Hewitt 1996) and leaves characteristic signatures in the genome of modern moose. Moose in Eurasia underwent 2 distinct, recent population expansions (Hundertmark et al. 2002b). Any other historic population processes preceding those expansions are not detectable because low population sizes eliminated much of the genetic variation present in the pre-bottleneck populations, and hence no signature from those times exists in the present genome. By applying a molecular clock to those expansion data, Hundertmark et al. (2002b) estimated that the expansions occurred approximately 160 140 120 100 80 60 40 20 0 2 0 -2 -4 -6 -8 -10 Thousands of years ago Te m p e ra tu re d i ff e re n c e ( C º) Fig. 6. Representation of mean global tempera- tures during the last 160,000 years relative to mean temperature in 1900. Negative tempera- ture differences indicate periods colder than today. The 2 glacial maxima of the last ice age are indicated by arrows. Estimated dates of moose population expansion are indicated by dashed lines and correspond to periods of warming associated with glacial retreat and northward advance of the boreal forest in Eurasia. Temperature profile adapted from http://gcrio.ciesin.org/CONSEQUNCES/win- ter96/article1-fig3.html. HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 112 ity in composition of mtDNA haplotypes. As noted previously, North American sub- species are distinct from European and Asian subspecies (Fig. 2) and none of the Asian haplotypes in the North American haplogroup were found in the Russian Far East. All haplotypes found in the Russian Far East (Magadan Oblast) are restricted to haplogroup 2 (Fig. 3), which contains all European haplotypes. A likely colonization scenario entails closely related moose from central Asia colonizing both Europe and North America. Lack of genetic similarity between moose in Alaska and the Russian Far East is inconsistent with the scenario proposed by Hundertmark et al. (2002b) concerning a colonizing wave of moose traveling from Asia to North America through Beringia. A single wave of moose colonizing North America through Beringia would have left genetically similar populations on either side of the Bering Strait after the Bering land bridge flooded. Yet, ages of subfossil re- mains of moose from North America indi- cate clearly that A. alces was present in Alaska prior to anywhere else on the conti- nent (Guthrie 1990, Hundertmark et al. 2003), unequivocally supporting an entry through Beringia. One hypothesis that accounts for this seeming paradox is that 1 or both of those populations underwent population bot- tlenecks shortly after the colonization of North America, and have only recently reestablished populations in those areas, leading to the presence of different genetic lineages in each. Moose in the Russian Far East show evidence of an expansion ap- proximately 1,200 years ago (Hundertmark et al. 2002b) and continue to expand their range toward the Bering Sea (Zheleznov 1993). 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 after the retreat of ice sheets from the last ice age (Cronin 1992). Similarly, no variation was 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 America were established as a result of a single entry into the continent, and that entry occurred during the population expansion of moose 14,000 years ago at the end of the last ice age, just before the closure of the Bering land bridge (Guthrie 1995, Hundertmark et al. 2002b). A recent entry into North America is the only conclusion that is con- sistent with limited variation in the mtDNA control region both within North America and between North America and Eurasia. If moose had existed in 4 separate refugia in North America during the last ice age, as suggested by Peterson (1955), or had en- tered North America from Asia more than once, a more distant common ancestor would be indicated. The timing of the entry is supported not only by genetic data but also by the distribution of suitable moose habitat at the end of the last ice age. The cold, dry grassland habitat that prevailed in Beringia for most of the last ice age was unsuitable for moose and was replaced by boreal forest only within the last 14,000 years (Guthrie 1995). Evidence from mtDNA variation also indicates that North American moose did not originate in Beringia, as some have speculated (Cronin 1992, Geist 1998), or recolonize the Russian Far East from North America (Coady 1982). Moose in North America are not closely related to moose on the western side of the Bering Strait (Rus- sian Far East). If those moose were once part of the same population recently sepa- rated by the flooding of the Bering land bridge, we would still expect to find similar- ALCES VOL. 40, 2004 MOOSE GENETICS - HUNDERTMARK AND BOWYER 113 indicative of a bottleneck notwithstanding the moderate levels of allozyme diversity reported for Alaskan moose by Hundertmark et al. (1992). Diversity of mtDNA can be reduced to a much greater degree by a bottleneck than diversity of nuclear DNA because mtDNA is 4 times more sensitive to genetic drift due to its haploid, uniparental mode of inheritance (Birky et al. 1983). Simultaneous bottlenecks in moose from both sides of the Bering Strait suggest a widespread causal factor. Recent studies have found evidence of significant biotic effects of climate reversals in Beringia af- ter flooding of the Bering land bridge (Elias 2000, Mason et al. 2001, Anderson et al. 2002). Those effects offer an intriguing mechanism for bottlenecks in Beringian moose populations. The greatest variation in mtDNA in North American moose occurs within the range of A. a. andersoni (Hundertmark et al. 2003). Alces a. shirasi from Colorado exhibited no diversity and A. a. gigas and A. a. americana exhibited very little diversity. If the paucity of mitochondrial diversity in Alaska is due to a bottleneck and recent expansion, those data would be consistent with the serial-founder-events hypothesis o f N o r t h A m e r i c a n c o l o n i z a t i o n (Hundertmark et al. 1992). The pattern of colonization of North America undoubtedly was influenced by the retreating glaciers and may have had s o m e e f f e c t o n g e n e t i c s t r u c t u r e (Hundertmark et al. 2003). Based on the r e c o n s t r u c t i o n o f t h e r e t r e a t o f t h e Laurentide ice sheet by Dyke and Prest (1987), we offer the following scenario of colonization. At the last glacial maximum, the Cordilleran and Laurentide ice sheets created an effective barrier between east- ern Beringia (Alaska) and other parts of the continent (Fig. 5). As glaciers retreated, a corridor opened on the eastern slopes of the Rocky Mountains allowing passage to the south. By 10,000 years ago, western Canada was ice-free but central and eastern Canada remained covered by the Laurentide ice sheet and large proglacial lakes (Fig. 7). Passage to eastern Canada north of the Great Lakes was impossible at this time and the only dispersal corridor was south of the lakes. By 8,400 years ago, moose arriving in the eastern continent could have dis- persed westward north of the lakes, skirting the southern shores of the proglacial lakes to the north, and come into secondary con- tact with moose from the west once the proglacial lakes receded. Moose in the e a s t e r n p a r t o f t h e c o n t i n e n t (A. a. americana) would have been on the end of a series of founder events, explaining their low 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 Great Lakes and Hudson Bay. Morphological Adaptation Moose of the Pleistocene and those that entered North America at the beginning of the Holocene were significantly larger than those living today, a trait shared with other northern ruminants (Guthrie 1984). Guthrie (1984) proposed that the reduction in body size was an adaptation to changes in sea- sonal forage availability that occurred as a result of climate amelioration at the end of the last ice age. The ability of moose to respond to a rapidly changing environment belies the relatively low levels of genetic variation documented by the studies we have reviewed and demonstrates that evo- lutionary potential is not easily predicted solely by genetic variability but ultimately is determined by the presence of adaptive genetic variation and heritability of traits that improve fitness (Lynch 1996). A general reduction in body size is not the only change to occur since the coloniza- t i o n o f N o r t h A m e r i c a . M o o s e i n HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 114 Fig. 7. Coverage of North America by the Cordilleran and Laurentide ice sheets and proglacial lakes at 14,000, 10,000, and 8,400 years ago (adapted from Dyke and Prest 1987). North America exhibit many differences in behavior and morphology. Alaskan moose are perhaps the most divergent; they exhibit a degree of sociality not observed else- where (Molvar and Bowyer 1994) and have more distinctive body markings, also indica- tive of increased sociality (Bowyer et al. 1991). Molvar and Bowyer (1994) sug- gested that moose in Alaska have evolved sociality recently as a response to living in open environments. Adaptation to open environments also applies to their mating system, which is harem-based. Harem mating is adaptive in open environments (Hirth 1977) where a male can protect a harem from competitors. Moose elsewhere in North America exhibit a tending-bond system of mating, which is adaptive for forested environments. Moose in Alaska and Siberia exhibit the largest body size of moose in North America and Eurasia, respectively. The similar ap- pearance of moose occurring on either side of the Bering Strait has caused some inves- tigators to consider them the same subspe- cies (e.g., Telfer 1984). As moose from those 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 to open, northern habitats by increasing body size. Adaptation to open habitats was dem- onstrated with a multivariate analysis of antler size among moose inhabiting differ- ent areas and habitats in Alaska (Bowyer et al. 2002). Those moose inhabiting open habitats (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 of their range in North America (A. a. shirasi) and Asia (A. a. cameloides) are similar; exhibiting small body and antler size (Geist 1998). Bubenik (1998) explained that simi- larity by proposing a second entry into North America by Asian moose—an entry that bypassed Beringia by traveling along the southern coast of Alaska. Neither genetic nor fossil data support that hypothesis (Guthrie 1990, Hundertmark et al. 2002a,b, 2003). GENETIC EFFECTS OF MANAGEMENT To this point we have discussed distri- bution of genetic and morphological diver- sity over space and time in the context of genetic drift and selection for locally adap- tive traits. Those patterns are developed over relatively long periods of time and are integral to the process of evolution. Genetic ALCES VOL. 40, 2004 MOOSE GENETICS - HUNDERTMARK AND BOWYER 115 change also can occur over short periods due to human influences, notably harvest management, and those changes may have unintended and undesirable consequences on individuals and populations (Harris et al. 2002) and therefore are important to recog- nize. Although it might be assumed that a well-designed harvest plan acts in a random fashion on genetic makeup of individuals, in reality even a managed harvest can be a highly 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 the extent of genetic drift and inbreeding in populations: effective population size and generation interval, respectively. Hunt- ing strategies were defined by different probabilities of harvest for both juveniles and adult females, and resulted in stable populations with decreased generation in- tervals and effective sizes compared with unhunted populations. Moreover, temporal changes in genetic diversity differed for different harvest strategies but always de- creased. Thus, Ryman et al. (1981) demon- strated that improperly designed harvest regimes can affect genetic characteristics of populations and by extension may have an influence on evolutionary potential. Con- versely, Cronin et al. (2001) detected no differences in numbers of alleles or levels of heterozygosity for 5 microsatellite loci among 3 moose populations in Quebec, 1 heavily hunted, 1 lightly hunted, and 1 not hunted. Another critical factor in management is the effect of harvest on genetic loci underlying characters having a direct effect on reproductive fitness, e.g., antler size in moose. Controlling harvest by defining legal 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 to evaluate genetic effects of the selective harvest system in Alaska, Hundertmark et al. (1993, 1998) modeled moose populations subject to harvest strategies employing dif- ferent definitions of legal males. They concluded that selective harvest systems could result in allele frequency changes at loci coding for antler characteristics (Hundertmark et al. 1993) and that the position 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). Those results indicated that limiting harvest to moose with large antlers could cause a genetically based decrease in antler size over time. Such a reduction in adaptive genetic variation runs counter to general conservation goals (Lynch 1996). A stun- ning example of the effect of harvest on fitness traits was recently reported by Coltman et al. (2003), who documented significant genetic effects on horn size and b o d y m a s s i n b i g h o r n s h e e p ( O v i s canadensis) as a result of selective harvest of males with large horns. Detecting potential changes in genetic composition of moose as they respond to various anthropogenic influences, whether related to management or to changes in the environment, is a difficult task. Nonethe- less, it is an important area of investigation and deserves attention. Modeling exercises and studies of genetic variation have not addressed interrelationships of moose populations at fine scales. The effects of management and habitat alteration on proc- esses involved in maintenance of connec- tivity of moose populations, such as male- mediated gene flow via yearling dispersal are extremely important and should be de- scribed. Moose are highly adaptable ani- mals, but the intensive management of moose HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 116 populations and the environmental factors influencing their habitat (e.g., wildfire) may have unintended and significant conse- quences on the moose genome through a change in selective forces. 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PETERSON, and B. N. WHITE. 2003. Genetic variation and population structure of moose (Alces alces) at neutral and functional DNA loci. Canadian Journal of Zoology 81:670-683. ZHELEZNOV, N. K. 1993. Historic and current distribution of moose in the northeast USSR. Alces 29:213-218. HUNDERTMARK AND BOWYER - MOOSE GENETICS ALCES VOL. 40, 2004 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.