Association ofofWUdlifeand Wildlife and Human Society
- Biosphere Conservation 1 (2) :107 117,1998
Geographic variation in the mitochondrial DNA of Steller sea lions: Haplotype diversity and endemism in the Kuri1 Islands
John W. Bickhami', Thomas R. Loughlin2, Jefftey K. Wickliffei, and Vladimir N. Burkanov3
i Departm ent of Mldlijle and flsheries Sciences,1lexas A&A( UhiversiC};College Station, llzxas,7rs43 UM
' LGL Ecotogicat Genetic& Ihc.1410 Cavitt St., Bryan,lhxas 77801 U{L4
21Vlational Mbrine Mbmmal Laboratot)l IVketional Mdrine Iilsheries Service, 7600 Sand Point Jlhy IVE, Seattlq Plashington 98115 Usa
3Ktimchatrybvod Cbmmittee ofFlshet y qfRussia, Prospect 1tybakov 1SL4, Petmpavlovsk-KbmchatskM Russia683024
Abstract Nucleotide sequence analysis ofa 238 base-pair segment of thc mitochendrial control region for 392 Ste]ler sea Iions (Eumetopias J'ubatus) from rookeries across nearly the entire distributional range of the species supports the hypothesis of two genetically differentiated stocks. An eastern stock includes rookeries in California, Oregon, British Columbia, and southeastern Alaska. A western stock includes rookeries in Prince William Sound, the Bering Sea, Central Gulf of Ataska, INbstern Gulf of Alaska, Eastern Aleutian Islands, Central Aleutian Islands, Russia (Commander Islands and Karnchatka), and the Kuril Islands. The distribution of haplotypes anda phyloge- netic analysis of the haplotypes provides evidence for the reconstruction of the evolutionary history of the popula- tions. Steller sea tions diyerged genetica]ly as the result of being isolated in at least two, and possibly three, glacial
refugia, 11he data indicate that females have a relatiyely high level ofphilopatTy and the contrel region has a rapid
rate ofevolution, which has resulted in relatively high levels of haplotype endemism in some areas. In particular, the
Kuril Islands appear to be highly variable with rnany low-frequency haplotypes unique to that area. Key words: Steller sea lions, EumetopiasjubattLs, milochondrial DNA, phylogeography, genetic stoek assessement
The Steller sea lion (Eumetopiasjubatus) is ern stock as endangered in the United States in 1997.
distributed across the North Pacific rim from the is- There are two Tecognized stocks of Steller sea 1ions.
land ofHokkaido, Japan, to southern Califbrnia, This An eastern stock ranges from California to southeast-
species was histoTically abundant with an estimated ern Alaska and a western steck ranges from Cape Suck-
tota] population of 240,OOO to 300,OOO during the ling to Japan, The western stock, which has histori-
1960s (Kenyon & Rice, 1961), Hewever, since that cally comprised the great majority of sea lions, has
time the species has experienced a steady decline with declined whereas the eastern stock has remained rela-
an estirnated total species population of 116,OOO in tively stable in numbers. Previous genetic studies
1989 (Leughlin et al., 1984, 1987, 1992) when the (Bickham et al., 1996b) have shown that these two
most complete range-wide survey was taken, The stocks are genetically divergent with respect to the ma- populatien within the United States has fallen from ternally inherited mitochondrial DNA (mtDNA). 192,OOO in the 1960s to 52,200 in 1994 (Anonymous,However, the previous genetic studies did not encom- 1995) and has Tesulted in the classification of the west- pass the entire range of the species and questions re-
11iis article was presented at the lbdo (Ste"er sea lion) Symposium, Sapporo, March, 1997, organized by Ohtaishi, N. and K, Whda,
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mained about the genetic relationships of certain popu- n = 20, Raykoke Island, n = 21, Antsiferova Island, n
especially the rookeries the western = lations, in far por- 15. CENTRAL ALEUTIAN ISLANDS; Ogchul
tion of the species range. This study reports additional Is]and, n = 10, YUnaska Island, n = 1O, Seguam Island,
data from mtDNA control-region sequences from 191 n = 10, Amchitka Island, Column Rock, n = 10, Kiska
Steller sea lions taken from rookeries in the Kuril Is- Island, Lief Cove, n = 10, Gramp Rocks, n = 10.
lands, Central Aleutian Islands, the Bering Sea, Prince BERING SEA; Walrus Island, n = 18. PRINCE WIL-
William SDund, British Columbia, and northcrn Cali- LIAM SOUND; Seal Rocks, n = 10, VVbodcd Island,
fornia. None of these regions were represented in the n = 10. BRITISH COLUMBIA; no exact ]ocality, n =
study of Bickham et al, (1996b). 5. NOIU'HERN CALIFORNIA; St. George Reeg n =
10. All samplesweTe taken nondestructively from in-
MMERIALS AND METHODS dividua]s collected at rookeries during the breeding
season.
Skin biopsies were taken from 191 Stel]er sea lions Gcnomic DNA was extracted (Maniatis ct al., and preserved in a so}ution of saturated NaCl with 20% 1982), and an approximately 450 base pair (bp) prod- dimethy]sulfoxide (DMSO) at room temperature uct of the mitochondrial control-region was amplified (Amos & Hoelzel, 1991), Six pepulations (grouped using polymerase chain-reaction primcrs LGL 283 and localities)were examined as fo11ows (Fig. 1): KURIL LGL 1115 as detailed by Bickham et al. (1996a,
ISLANDS; Srednego Island, n = 22, Lovushki Island, 1996b). Primer LGL 1115 was used as the sequenc-
'the F]g. 1. D]stnbutLonal runge of the Stel]er sea lion (shuded) ttnd ]ocat:on of the grouped ]ocahties used in the populution anal.vses grouped locaht]es {from west to east) are Kuril Islands (KUR). Comrnander Islunds and Kamchatka (RUS), centrul Alcutiun Islamds (CAL), eastern Aleutian Islands (EAL), western Gulf of Alaska (WGA). central Gulf of Alasku (CGA), Pribilof Islands in {he Bering Sea (BER), Pnnce Wil]iam Sound (PWS), southcastern Alasku (SEA), B"tish Columbia (BRC), Orcgon (ORE), and northern CuTLfor- nia (NCA) Data from KUR. CAL, BER, PWS, BRC, and NCA ure presented in this paper, the other ]ocalities were reported by Biekbam et al. (1996b).
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ing to obtain a 238 bp primer sequence using auto- for hapletype A has bcen deposited in Gea Bank (ac-
sequcnce technology employing dye labelled termi- cession no. AF041380).
nators (Carr & Marshall, 1991; Fer] et al., 1991). All Phylogenetic analysis of all haploytpes, including sequences were generated using an ABI 373A auto- those reported previously (Bickham et al., 1996b),
mated sequencer and sequences were edited and were analyzed from Tamura-Nei distances using the
aligned using the SeqEd program. Haplotypes wcre neighbor-joining method in the MEGA program. identifiedaccording to their uniquc combinations of Nucleon-diversity estimates were generated using
nucleotides within this 238 bp region. The sequence equation 7 in Nei and Tajima (1981) for each grouped
Tab]e 1. Numbers of individuuls of each haplotype observed are presented for each of the four Kuril Island rookeries Hnd fer the fol]owing grouped localities: central Aleulian Is]ands (CAL), Bering Sea (BER), Prince William Sound (PWS), British Columbia (BRC). and northern California (NCA). bocuLity Haplotype Sfednego Is. Lovushki Is, Raikoke Is,Antiserova ls.CAL BER PWS BRCNCA AEGHLMNQRsTwxzBBccDDEEFFHHwwAAABBBCCCDDDEEEFFFGGGHHHIIIJIJKKKLLLMMMNNNoooPPPQQQRRRsssTTrUUUvyvwwWTbtal5 1 6 22 11 1 2 2 41111 1
1
2 19113312144221151511 3113224
l3
8 61 5 2 1
1 1 1 21
1 5 4
l
1 2 1!
11311 11
2 1111 l
1111
11115 121
22 20 60 18 20 s to
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紛 O 雷 忖 り 卜 卜 自 ゐ 曽 O 団 く ［ U 二 緡 目 』 国 ‘ σ
ゆ N 側 ” 卜 UU り 凵 凵 芒
の ． oh （ き 閃 U ［〔二 roor h ま ひ 口 ヨ隔二 ℃ ［． 口 rn O ｛ のo 三 o 。 尸曽 σ 薛 E く ． 囗≦ 四 o 三 レ 凵 価 荳 uh 国 試 rnPト U 一 三 皀 三 峯 口 ト 卜 卜 卜 〇 」 り r o 9 。 饗 く ‘ h こ 。 o 窓 r醤 σ t ｛ 冒 OE6D N 甲 r鴇 O ｛ く く く く ω 蓬 曽 匹 で 〜 rrNr9r 凵 卜 凵 』− 黯 Q ◎ N 門 − 囚 凵 ＜ q t 《 に の ε 民 ξ 卜 ≧ ［言 匹 翰 ℃ ＝ ト 嚆 呈 霊 ． ε 穹 q 呼 。う 二 U ト ＝ ‘ O 詈 ヨ 9 。 靄n 。 の 凶 ＝ O α 嘱 O ユ 。 O N ℃ 薯 ＝ U ｛ 醤 。 ｛ ｛ O 【。
O 曁 可 翌O で 「 凵 卜 コ 【： ロ ［O 量 8F ∪ P 」 卜 卜 卜 髭 雪 詰 円 ＞ 9 ド 話 U 凵 凵 Uu QOn ・ 。 ま U ト あ O 三 ト 畷 ℃ 窮 召 U 卜 レ 忌 ← 二 唱 ℃ 婁 」 凵 凵 凵 9 口 凵 口 u 口 口 凵 u の仍 口 U 口 帽 瓢 u 「 ． 匚（ 田 レ 口 2 』 ［ ま 卜 O2 卜 訂 9 」諺 ． O ト 目 O ヨ 。 ひ あ nO く O ” Eo 鬢 至 叭 ト 凵 占の2 U uv 自コ ト ニ ） 頃 ト り シ 台 o 噂 三 頃 ｛ 口 覧謂 』 臣 ヨ N U ＜ 。 卜 P ZO 。冫 h 渇 ｛ O 切 冩 牙 ＝ ℃ 掣 三 ト 凵 uv ＝ O 昭 ‘り 0 口 F ト ← 卜 卜 ト ト O ≧ 二 閉 rN Σ 〇 ． 雪 雪 三 哩 囗 OOOUUU No ヨ 国 醗 § 耋 ≡ ミ 鬘 ヨ 堊 萋 § k § 鞴 E § 耋 耋 蟇 辜 N 誉 喜 一 8 瑠 司 』網 ” 吋 卜 鬢
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locality. Population differentiationwas assessed us- 113, 124, 142, 145, 223, and 226) were not variabie in l
ing Nei identity and Nei (1972)genetic (1978)unbi- thc samples reported by Bickham et al, (1996b). A ased identity of the haplotype frequencies genetic for total of 44 haplotypes were observed (Table 1), of
localities in this grouped presented paper and in which 23 have not been previously reported in our stud- Bickham et al. using (1996a) the program BIOSYS-1 ies (Bickham et al., 1996b, in press). In combination
& Selander, 1981). (SwoffOrd Becauseof the limita- with the previous studies, we have now observed a
tions of this in only allowing a maximum of program total of 78 haplotypes in Steller sea lions (A-Z, AA- 30 alleles lecus, we combined the rookeries per from ZZ, and AAA-ZZZ). With regard to thc geographic
British Columbiawith those of southeastern Alaska distribution of these haplotypes, therc appears to be
and the rookeries from northern Californiawith those four distinct patterns. Forty-nine haplotypcs are known
from Oregon et al,, 1996b). A (Bickham hap}oid from only a single grouped locality. Often, thcse are single-]ocus mode} was used in which the unique al]e- found in very low frequecies. For examplc, 41
lesfrom al] grouped localities were combined into a haplotypes are known from only a single individual,
single dummy allele for each grouped locality, thus six haplotypes are known from two individuals, one
reducing the number of alleles to 30. Cluster analysis haplotype is known from three individuals, and one of the genetic distances for the grouped localities was haplotype is known from seven individua]s. A second
performed using the unweighted-pair-group method pattern is found in two haplotypes, A and BB, which
(UPGMA) in BIOSYS-1. An additional analysis of are nearly ubiquitous in theirdistribution. Both ofthesc differentiation population was performed in which haplotypes are fbund in the highest frequencies in the
identities arnong the four rookeries of the Kuril genetic Kuril Islands and the other Russian grouped locality. Islandswerc and relationships generated among popu- A third pattcrn includes haplotypes that are found in
lations were analyzed by a UPGMA cluster analysis. more than one region, but restricted in distribution to
either the eastern or western stock. This is the sec- RESUI;TS ond-most commonly observed pattern, comprising 21
haplotypes. A fourth pattern inc]udes only haplotypes
Sequences were obtained fromthe mitochondrial S and FF, which are primarily distributed among the
control region for191 Steller sea liens. Within the western localities, but each with a single individual
238 bp regien analyzed, there were a total of 38 vari- from southeastern Alaska. These four patterns are able of which nine positions, (positions56, 68, 86, apparent in the data reported in Bickham et al. (1996b),
Tbble 3.Matrix of genetic identity for 1O grouped localities of Stellcr sea lions. Above diagonu] is Nei's (1978) unbiased genetic identity and below the diagona] is Nei's <1972) genetic ldentity.
Population 123456789IO
1. KUR2. O.69 022O.44O.28O.56O,81O.24O.55O.70O.72O.22o.soO.83O.84O.92O.18O.46O.67O.74O.92O.97O.34O.61O,68O,74O.63O,73O.55O.27O.34O.11O.!4O.14O.12O.11O.16O.20O.25O,04O.09O.06O,07O,05e,13O,40
RUS3. e,66O.22O.26023021O.16e.31026O.20
CAL4. O.41O.51O.51O.47O.41O,54O.32O,23
EAL5. O.75O.66O.79O,61O,61o.leO.04
WGA6. O.66O.7SO.66O.65O.13O.09 CGA7. O.86O.82O,5SO.13O.06 BER8, O.88O,6SO.11e,o7 PWS9, O.47O.10O.04
SEA/BRC O.14O.12
10. 0REXNCA O.39
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as well as in the data set reported here. ' Table 2 reports the sequence data for the 38 vari- able for haplotypes AAA to These positions ZZZ. data ' in combination with sequences reported for haplotypes A toZ and AA to by Bickham ZZ et al. (1996a), were analyzed phylogenetically to determine whether or not maternallineagesaregeographicallysequestered(Fig. 2),Itisclear from this tTee that most ofthe haplotypes representative of the eastern stock of Steller sea lions branch out from the base of the tree. Thus, it appears fromthis analysis that the eastern stock haplotypes are mostly plesiomorphic in nature. On the other hand, the haplotypes characteristic of the western stock all trace their ancestry back to a single common ancestor that forms the base of a relatively derived and highly diverse lineage. This Iineage is paraphyletic in the sense that it also includes some haplotypes found in the eastern portion of the spccies range (B, P, Q, R, and UU) as well as the two widespread haplotypes A
and BB. These new data do not substantially change the tree reported by Bickham et al. (1996b), and in factcan be considered to bc in strong support of their conc]usions. Pair-wise genetic identity estimates for ten grouped localitieswere obtained using Nei (1972) genetic iden- tityand Nei (1978) unbiased genetic identity (Table 3; 392 Steller sea ]ions coalected from rookeries dur- ing the breeding season, including animals reported in this study and by Bickharn et al., 1996b). UPGMA cluster analyses were performed on these estimates 3).The (Fig. different genetic identity procedures pro- duced identically branched trees. IXvo very distinct
clusters, representing the eastern and westcrn stocks ef Bickham et al. (1996b), c]ustcr at a level of O,13
genetic identity. The eastern stock inclttdes only the two grouped localities southeastern AlaskalBritish Columbia (SEAfBRC) and Oregonlnorthern Califor-
wtsctwPeHXATxxN nia (ORE/NCA) which clusteT at a ]evel ofO.39. The EASTEnN7rwnON western c]uster of populations includes two woEwn HuntwEs k gToups which cluster at a level of O,35. The Kuril Islands Fig, 2. Neighbor-joining lree of 78 haplotypes of (KUR) and the other Russian rookeries (RUS) ciuster Ste]]er sea liens based upon lhrnura-Nei dis- at O.65and are distinct tancesofthenucleotidesequenceofu238-bp from the populations in the segrnent of the mitochondrial control region, Bering Sea (BER), the central (CAL) and easteTn
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KURRUSCMEALWGACGABERpwsSEABRCORENCA
1
.OO .10 .20 .30 .40 .SO .60 .70 .SO .oo 1.00
's Fig. 3. Cluster unluysis (UPGMA) of Nei (1972) genetic ldentity for IO grouped localities ef StelLer sea ]ions,
(EAL) Aleutian Islands, Prince Williarn Sound (PWS), ANTS h = O.943. and the wcstern (WGA) and central (CGA) Gulf of Alaska, which clusteT at O,58. Among these latter popu- DISCUSSION
lations, which rnake up the central Tange of the spe-
cies, it can be seen that the Bering Sea population clus- The data presented in this paper extend and con-
closely with the of the ters Gulf Alaska populations, firm the conclusions of Bickham et al. (1996b) regard- Aleutian populations cluster together, and the Prince ing the genetic difTerentiation of the eastern and west- Wi]liam Sound popu]ation is the most distinct among ern populations of Steller sea lions. Thc difference in
this group. mtDNA haplotype frequencies between the southeast- Pair-wise genetic identity estimates were also pro- ern A]aska population and the Gulf of Alaska popula-
duced for the four rookeries within the Kuril Is]ands tions comprises the major phylogeographic feature of (Table 4). UPGMA cluster analysis for these identity this species. Bickham et al. (1996b) concluded that estimates clearly show that Antsiferova Island (ANTS) this phy]ogeographic pattern likely resulted from ge-
is highly distinct from the other three islands in this netic divergence during the Pleistocene when the two
group (Figs. 4 & 5). Srednego (SRED) and Raykoke stocks ef Steller sea lions were isolated in separate
(RAYK) Islands c]uster at an identity of O.90, fbllowed glacial refugia in Bcringia and the Pacific Northwcst
by Lovushki (LOV) Island at an identity of O.72. How- of North America. However, a consideTation of the ever, AntsiferovaIsland clusters at an identity of O.29. analyscs presented in this paper provides a somewhat
This appears to be duc in part to the absence of a]leles different perspcctive. The two widespread haplotypes,
A and AAA in the Antsiferova samp]es, whereas these A and BB, are found distributed across the entire range
alleles are at rather high frequencies at the other three
Islands (Table 1). Rible4,MatrixefgeneticidentityforfollrStellersealionrooker-
Nucleon diversity estimates were high among al] ies from the KuriL Is]ands. Above diagonal is Nei's (1978) unbiased gcnetic identity and below the diagonu] is Nei's rookeries and grouped localities examincd. Estimates (1972) genetic identity. for grouped localities were: KURh = O,874, CAL h = Population 1 2 3 4 O.854, BER h = O,869, PWS h = O.916, BRC h = O.9, 1. SRED2, O.84 O,94O.86 O,66O.61O,50 NCA h = O.844. Nucleon divcrsity estimates among LOVU3, O,7SO,85O,55 the four rookeries of the Kuril Islands were: SRED h RAYK4. O,76o.so
= = = O.823, LOVU h O,863,RAYK h O.852,and ANrs O.40
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L' ' L'S"''':: tttttttt :.,:Li/'']'i.:,.s:..',.:I'.i;g ,,,, 1 : ,/;.,',::';1: /,,/..,,...ii. ' Rus,sja,...1, ' --t ･.tft. t. . li,: .･r:. .･,1.,. t tt ttt :tt:tt .:･･:.･b.,Z' :[,･･･ta,/･; 't.1./ttrt}t" ''･s..･1fl･,. ../,t t " ttt:.l./.t... ･q e .' ･/.:T ,',.･1 t t ttttttltt. '" tt ･･,-･1･"" ttt:t::- e ttttt il'-1 s.:... ･-/ ･"･,･'¢ ' 'setfa Okhotsk Sea tt:/if. .o l.,:;･, 1,& . "ilit'" ,f'r-:･f:･,':::･:1'11"1'1･ ･i:･.... t : '1tttt ":"1' i ,,･,s.,1 tt tttt ttttv tt t ttttt ttt.:t Bering tttttttt-tt ":･/ '･ khatin 1. .';･T -tttt ' :E t::,./,/:1. Sea L.'E ' Antsiferovo S. ' ./:..i'i ･.'s[ Rayko!sg..!.t..N'? ':･: /l .t t:: tl..:. , i. ?:/tttttt;-:tt .)-Lovushki , r 'it:t "NSrednego t. tt t e- ..,,fr
:･:-:,･ ,,ts;ilf･
Pacific Ocean .
t;'/'ttt'
Fig. 4. Map of the Kuril Islands showing the locations of the fouT Steller sea Lion rookeries which w ¢ re sampled in this study,
of the species, from the Kuril Islands to California. It the westcrn popu]ations. If this were the case, the de-
is of interest that both ofthese haplotypes are found at gree of isolation between the animals in this Asian refi
higher frequencies in the Kuril Islands and the other ugium and those in the Beringian refugium was not as
Russian rookeries than anywhere else in the range of great as between thesc and the Pacific Northwest ref
the species. This is suggestive of a pattcrn of post- uglurn. Pleistocene dispersal from the Asian populations east- This study reports data from 60 animals represent-
ward across the Aleutians, Gulfof Alaska, to Califor- ing six rookeries in the central Neutian Islands. In all
nia. Thus, Asia, rather than Beringia, mighthave been cases the haplotypes frem these animals arc consis-
the location of the Pleistocene refugium for the west- tent with the results of Bickham et al. (1996b). It is ern stock. clear from the genetic identity estimates that the east- Another interpretation ofthis pattern of geographic crn and central Aleutian Island populations of Stel}er di･vergence is that as many as two separate glacial refu- sea lions are closely related (Fig. 1). Moreover, there
gia were occupied by the ancestors of the western stock. is rather 1ittle endemism in this region. Thcrc are only
This is suggested by the fact that the Russian and Kuril 10 haplotypes that are unique to the Neutian Is]ands,
Island populations are quite distinct from the rest of from a total samplc size of 100 individuals. This com-
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to 18 haplotypes restricted in distribution pares to ship of this population to the eastern stock and thc
Russia and the Kuril Island populations(whichrepre- three individuals observed by Bickham et al. (1996b) sent 122 samples), and 19 haplotypes found only in most likely represented eastern stock individuals that the eastern stock populations (59 individuals). had wandcred far away from their natal rookeries but
We studied 18 animals fromWalrus Island,a rook- would not likely Temain in this area during the repre-
ery in the Pribilof Islands of the Bering Sea. This popu- ductive season. lationhas a strong affinity to the Gulf of Alaska popu- A separate analysis of four rookeries of the Kuril
lations (Fig. 1). It is reasonable to assume that this Islands was eonducted in order to determine to what
rookery was colonized by females from the Gulf of degree mtDNA haplotypes are useful to distinguish
Alaska, and that this co]onization was relatively re- among nearby rookeries. The most distant of the four cent. VVe observed only two unique haploytypes (EEE rookeries, Antsiferova Island, is clearly the most ge- and JJJ)in the Bering Sea population. Each of these netica}]y divergent, clusteTing at a level of O.59 ge-
haplotypes representcd a single individua]. netic identity, whcrcas the other three rookeries clus-
Bickham et al. (1996b) examincd thTee individuals ter at O.85 genetic identity (Fig. 3). Antsiferova Is-
from Prince William Sound that were taken outside of land differed considerably from the other three islands
the breeding season. They concluded that these indi- in frequencies for some haplotypes, such as A and viduals had haplotypes that wcrc characteristic of the AAA, as weH as in possessing six haplotypes not ob- eastern stock, not the western stock which comprises served in thc otheT three Kuril Island rookeries (Table
the adjacent Gulf of A]aska populations, Moreover, 1). It should be noted that each of these rookeries
Lidicker et al, evidence from allozymes at lcast =1-4) (1981)found possess one (range unique haplotype. that the Prince William Sound population differed Therefore, these data show that in at ]east sorne in- slightly the of from Gulf Alaska populations, We ex- stances the mtDNA haplotypes might be useful in
amined 20 Steller sea lions from two rookeTies in microgcographic comparisons of genetic diveTgence
Prince William Sound and found that their haplotypes in Steller sea lions.
were either broadly distributed (BB) or characteristic The data prescnted in this paper extend and con- ofthe western stock (seven haplotypes). Only asingle firm the conclusions of Bickham et al. (1996b) that haplotype was observed that was unique to Prince there exists two genetical]y well-differentiated stocks Wi]liam Sound (FFF), and this haplotype is phyloge- of Steller sea lions, an eastern and a western stock. netically related to western the stock haploytpes (Fig. Among the westem stock, which has decl ined dramati- 1).Therefore,no cvidcnce was seen for any relation- ca]ly over the past threc decades, the rookeries of the
SRED
RAYK
LOVU
ANTS
.4e.46.52.5S,64.70.76,S2.ss.941.00
Fig. 5. Cluster anuiysis{UPGMA) of Nei (1972) genetic idcntity for the four Stel]er sea lion rookcries frorn the Kuril Islunds,
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Kuril Islands appear to be the most distinct, possess- divergent population, as is the easteTn stock of Steller ing a high number of unique haplotypes. As reported sea lions. However, the Asian populations (E. I. Iutris in the studies of Bickham et al, (1996b), this species from the Kuril Islands and Medney Island) do not clus-
has a very high lcve] of mtDNA haplotype diversity. teT together separately from the E. t. kenyoni popula- A serious consideration in regard to the conservation tions, whereas sea lions from these same geogTaphic of this species is whether or not genetic diversity will areas are clearly distinct. Finally, the populations of
be eroded as a result of population decline. Bickham both sea otters and Steller sea lions from Prince Wil]-
et a]. (in press) examined mtDNA in Stcller sea lions iam Sound are surprisingly divergent from the nearby
collected in thc 1970s and compared nucleon diver- populations in the Gulf of Alaska and Aleutian Islands, sity estimates from that population to estimates de- with respect to mtDNA, Thus, although there are sorne ,
rived from samples collected in the 1990s from the differences in the biogeography of these two maTine
same area. It was concluded that haplotype diversity mammals, the similarities are striking and most likely
has remained high and that no statistically significant result from shared historicai events that havc similarly
changes have occurred in haplotype frequencies in spite shaped the patterns of popu]ation divergence seen of the drastic decline in numbers that has occuTred in arnong the living populations. the GulfofAlaska. However, based upon a statistical The data presented in this papcr further contTibute
model ofthe population decline, oveT thc next 30 years to our understanding of genetic variability in Steller
popu]ation density in some areas is expected to reach sea 1ions, a threatened and potentially endangered spe- a point whcrein the loss of genetic vaTiability is inevi- cies, It is encouraging that high }cvels of rntDNA vari-
table if the decline of this species cannot be stopped. ability are stil] apparent after three decades of severe
Thephy]ogeographicpatternsofpopulationdiffer-dec]ine. Data presented in this paper represent impor-
entiation in mtDNA of Steller sea lions is similar in tant base]ine information that might be useful in fu-
many respects to the patterns of mtDNA and morphol- ture monitoring efforts for some critical, and rcmote,
ogy in sea otters (Enhydra lutris). Sea otters have a populations of Ste]ler sea lions. similar geographic distribution to Steller sea ]ions,
being distributed from Hokkaido across the North ACKNOWLEDGMENTS
Pacific Rim to northern Mexico. There are three sub-
species recognized on the basis of morphological fea- We thank R. Stuart and J, Patton of LGL Ecologi-
tures, including E. I. tutris distributed from Hokkaido cal Genetics Inc., for assistance in thc laboratoTy.
through thc Kuril Islands to the Commander Is]ands. Funding was provided by the Nationa] Marine Fisher-
Enhydra L kenyoni is distributed throughout the Aleu- ies Service. This paper represents contribution no. 66
tian Islands, the Gulf of Alask, and southeastward to of the Center for Biosystematics and Biodiversity at
Oregon. Enirydra L nereis is found in California and Texas A&M University.
nothern Mexico. Thus, as in Steller sea lions there
appears to be three differentiated forms, one in Asia, REFERENCES
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