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Mini-review: distribution of the Mediterranean mussel Mytilus galloprovincialis (Bivalvia: Mytilidae) and hybrids in the Northeast Pacific.

ABSTRACT The non native Mediterranean mussel Mytilus galloprovincialis is broadly established in the northeast Pacific. Until recently, the coast north of Humboldt Bay, California, USA, was not considered a major zone of sympatry and hybridization with the native sibling species M. trossulus. However, M. galloprovincialis has been introduced in Washington, USA, and British Columbia, Canada. for aquaculture, has been collected from ballast water in-bound to Oregon, USA, and is now reported widely in Puget Sound, Washington. Here 1 review published reports of M. galloprovincialis alleles in the Northeast Pacific, including recent data showing that these alleles are more widespread and abundant in Washington than previously known. These results indicate the presence of a major zone of sympatry and hybridization in Washington waters that may be contiguous with the California zone. Because M. galloprovincialis has likely been introduced to the region on multiple occasions via multiple routes, it is unlikely that a sole source can be identified. Factors influencing the success and impacts of this now widespread invader remain to be investigated.

KEY WORDS: introduced marine species, hybridization, Pacific Northwest, Mytilus galloprovincialis

INTRODUCTION

The marine mussel genus Mytilus includes a complex of 3 sibling species, M. edulis L. 1758, M. trossulus Gould 1850, and M. galloprovincialis Lamarck 1819. All three are now globally widespread and form hybrid zones where they overlap (McDonald et al. 1991, Sarver & Foltz 1993, Hilbish et al. 2000). The role of human activity in establishing the global but disjunct distributions of these species has been addressed in terms of genetic evidence, fossil evidence, and the available introduction pathways. (e.g., McDonald et al. 1991, Carlton 1999, Daguin & Borsa 2000, Hilbish et al. 2000)

Certain features of Mytilus species make them likely candidates tot human-mediated introduction: their planktonic larval stage allows them to be passively transported in the ballast water of commercial ships (e.g., Carlton & Geller 1993), byssal threads produced by juveniles and adults allow transport on hard substrata including ship and boat hulls (Carlton & Hodder 1995, Apte et al. 2000), and their palatability and relative ease of culture has led to their widespread introduction for aquaculture (Heath el al. 1995, Couturier 2003 and references therein).

M. galloprovincialis is the most widely distributed of the three sibling species, and recent genetic analyses distinguish among multiple hypotheses for its origin and spread (Daguin & Borsa 2000). In the Northeast Pacific, M. galloprovincialis ranges from Mexico to central California, and recent surveys confirm its presence throughout the inner waters of Washington State (Suchanek et al. 1997, Anderson et al. 2002, present study). The origin, timing, and pathways of its introduction to Washington remain unclear, and it has likely been introduced on multiple occasions. Here, I summarize recent genetic analyses of Mytilus spp. distributions globally and in the northeast Pacific, provide additional sampling results from Washington State waters, review our current understanding of the M. galloprovincialis introduction to the region, and identify ecologic questions to be addressed concerning this introduction.

Global Mytilus Distributions

Because Mytilus sibling species and their hybrids cannot reliably be distinguished with morphologic characters alone, genetic analysis is required to determine their distributions and origins. M. edulis and M. galloprovincialis are the most closely related and M. trossulus is the most divergent according to genomic DNA (Beynon & Skibinski 1996, Eirin-Lopez et al. 2002, Martinez-Lage et al. 2002) and mtDNA analysis (Rawson & Hilbish 1995b, Quesada et al. 1998, Geller 1999, Hilbish et al. 2000). Two additional studies report evidence that may suggest that M. galloprovincialis is the most divergent of the three species (Wenne & Skibinski 1995, Varvio et al. 1988). However, the mtDNA-based species determinations in one study (Wenne & Skibinski 1995) may have been confounded by sex-specific differences, and the other study stated clearly that their allozyme analysis should not be taken to indicate relative relatedness among the species (Varvio et al. 1988).

The three sibling species have distinct but overlapping distributions. M. trossulus is circumpolar in the north Pacific, northwest Atlantic, and Baltic, but has not been unambiguously identified in the southern hemisphere (McDonald et al. 1991, Hilbish et al. 2000). M. edulis is found in the northeast and northwest Atlantic, and edulis-like mussels arc reported from South America (McDonald et al. 1991). M. edulis has also been introduced to British Columbia tot aquaculture (Heath et al. 1995). M. galloprovincialis is distributed throughout the Mediterranean and into the northeast Atlantic, with additional populations in California, Japan, South Africa, Australasia and Chile (McDonald et al. 1991, Sanjuan et al. 1997, Daguin & Borsa 2000, Hilbish et al. 2000). To account for its disjunct distribution, M. galloprovincialis has been proposed variously to be endemic to the Mediterranean and introduced in the north and south Pacific (Barsotti & Meluzzi 1968, McDonald et al. 1991, Carlton 1999), possibly endemic to the south Pacific (Koehn 1991, McDonald et al. 1991), and endemic to both the Pacific and Mediterranean (Sanjuan et al. 1997). These alternate hypotheses are comprehensively reviewed by Daguin and Borsa (2000) and Hilbish et al. (2000); the key points are summarized here.

Northern hemisphere populations of M. galloprovincialis in the Atlantic and the Mediterranean can be distinguished by allozyme (Quesada et al. 1995b, Sanjuan et al. 1997) and mtDNA analysis (Quesada et al. 1995a, Quesada et al. 1998, Ladoukakis et al. 2002). The Californian population is more closely related to the Mediterranean than to the Atlantic population in allozyme (McDonald & Koehn 1988, Sanjuan et al. 1997) and genomic DNA studies (Daguin & Borsa 2000). In the southern hemisphere, Mytilus sp. appear in fossil beds and middens, and genomic DNA analysis indicates that present-day populations arc closest to, but readily distinguished from, Mediterranean populations (Daguin & Borsa 2000, Hilbish et al. 2000).

The emerging evolutionary and historical picture that appears most consistent with genetic and geological data is that the genus Mytilus evolved in the north Pacific, that the M. trossulus stock migrated ~3.5 mya through the Bering Strait to the north Atlantic where the M. edulis stock arose, and that M. galloprovincialis subsequently diverged from M. edulis in the Mediterranean (Vet meij 1991, 1992; Daguin and Borsa 2000; Hilbish et al. 2000). Subsequently, both M. galloprovincialis and M. edulis migrated to the southern hemisphere (Vermeij 1991, 1992, Daguin & Borsa 2000, Hilbish et al. 2000). Since these early natural dispersal events, more recent translocations have occurred to California, southern Africa, and the northwest Pacific (Wilkins 1983, Grant & Cherry 1985. Lee & Morton 1985, McDonald & Koehn 1988, Inoue et al. 1997, Sanjuan et al. 1997, Daguin & Borsa 2000). Because none of these introductions is known to have been intentional, they most likely occurred accidentally via commercial ship ping transport. Mytilus species may also have been recently transported to the southern hemisphere by shipping; this remains to be determined.

Northeast Pacific Mytilus

The broad-scale distribution of Mytilus species along the Pacific coast of North America is well established. M. trossulus is currently found from Alaska south to Monterey Bay, California (~36 [degrees]N) and M. galloprovincialis from Mexico north to Humboldt Bay, California (~38 [degrees]N). An apparently stable hybrid zone extends between San Diego (~32 [degrees]N) and Humboldt Bay (McDonald & Koehn 1988. McDonald el al. 1991, Sarver & Foltz 1993). The congener M. californianus is a morphologically, genetically, and ecologically distinct species that is found on exposed shores along the entire coast (Sarver & Foltz 1993); it is not treated further here.

Until recently, only a handful of M. galloprovincialis and hybrids had been collected from Oregon to British Columbia, and the coastline north of Humboldt Bay was not considered a major zone of sympatry and hybridization (Heath et al. 1995, Rawson & Hilbish 1995a, Suchanek et al. 1997, Rawson et al. 1999). However, M. galloprovincialis has been widely introduced for aquaculture in Washington and British Columbia, and M. edulis to a lesser extent in British Columbia (Brooks 1991, Heath et al. 1995, Hilbish 1999, Anderson et al. 2002). In addition, M. galloprovincialis has been identified in ballast water loaded in Japan and scheduled for discharge in Oregon (Carlton & Gullet 1993, Geller et al. 1994, Suchanek et al. 1997). Given the large scale of both aquaculture and ship-mediated invasion pathways in the Pacific Northwest (Wonham & Carlton 2004), we might expect M. galloprovincialis (and possibly M. edulis) to be more widely distributed in these waters. Indeed, recent surveys of Puget Sound and the Strait of Juan de Fuca, Washington, indicate that M. galloprovincialis alleles are distributed broadly in the south and central sound and in the Strait of Juan de Fuca (Anderson et al. 2002, present study). Along the outer coast, M. galloprovincialis is reported from northern California and Oregon, but seems to be largely absent from Washington (Suchanek et al. 1997, Brooks 1991). Northeast Pacific records of M. galloprovincialis and hybrids are detailed here by province and state.

British Columbia

Heath et al. (1995) sampled 12 sites on Vancouver Island and the adjacent mainland (Fig. 1. Table 1). They found non native alleles belonging to either M. galloprovincialis or M. edulis at five sites from Yellow Island to Victoria. Because mussel aquaculture is continuing to develop in BC, new surveys in this region using species-specific markers are welcome.

[FIGURE 1 OMITTED]

Washington

The subtidal distribution of M. galloprovincialis alleles in Washington extends throughout the Strait of Juan de Fuca, the North Puget Trough, and Puget Sound (Fig. 2, see Table 1). M. galloprovincialis was identified as early as 1988 in the eastern strait (Brooks 1991), and extensive sampling in the straits and Puget Sound indicates it is now ubiquitous in this region (Anderson et al. 2002, present study). It has been found in the East, Main, and South Basins of Puget Sound, but not in Hood Canal, and appears less frequently in Northern Puget Trough (see Fig. 1, Table 1). Brooks (1991) found no M. galloprovincialis on the outer coast of Washington; one hybrid was reported from Tatoosh Island by Suchanek et al. (1997) but none was found there in recent sampling (present study; see Fig. 1, Table 1).

[FIGURE 2 OMITTED]

In this study, I made 16 collections totaling 390 individual Mytilus at 15 Washington sites from 1997 to 2000 (see Table 1). Subtidal mussels were collected by hand from public docks and marinas and one aquaculture farm. Ten of the docks and marinas were sampled during a rapid-assessment survey for introduced marine species (Cohen et al. 1998), and an additional four were sampled along the northern Olympic peninsula (see Fig. 1, Table 1). At each site, up to 15 mussels were collected by hand from underneath floating docks. Mussels were selected haphazardly, but because they were collected as visible and accessible among other fouling species, they tended to be large (all 3-10 cm long). Mussels in the same size range were also collected from suspended culture ropes at Taylor United Shellfish farm, Shelton, Washington. These included both cultured mussels (i.e., M. galloprovincialis seeded from hatchery stock) and natural-set mussels (see Table 1). Intertidal mussels (1-3 cm shell length, representing the largest mussels at the site) were collected from the rocky shores of Tatoosh Island at the entrance of the Strait of Juan de Fuca, and Saddlebag Island in Padilla Bay (see Fig. 1, Table 1). All specimens were stored at -10[degrees]C until identification.

Mussels were dissected and DNA was extracted from 0.5 g of gonad tissue following Geller et al. (1994). Polymerase chain reaction (PCR) amplification followed Suchanek et al. (1997) using the species-specific primers developed by Inoue et al. (1995). The PCR product was run on a 2% agarose gel: individuals homozygous for this marker exhibit a single band and heterozygotes exhibit bands of both parental species (Inoue et al. 1995, Suchanek et al. 1997, Wonham 2001). All heterozygotes are M. galloprovincialis x M. trossulus hybrids, whereas homozygotes may represent either pure or introgressed genomic DNA strains. Although introgression seems to be limited in these populations (Rawson et al. 1999), heterozygote frequencies nonetheless probably underestimate the relative abundance of hybrids. Reference DNA samples for each species were provided by J. Mitton, University of Colorado. For further collection and analysis details see Wonham (2001).

I found M. galloprovincialis genes in subtidal mussel samples throughout Puget Sound, the Strait of Juan de Fuca, and northern Puget Trough. Homozygote M. galloprovincialis and heterozygores were present at 4/4 marinas along the Strait of Juan de Fuca, and 6/8 marinas in Puget Sound (Figs. 1 and 2, see Table 1). Together they averaged of 22% of mussels in both regions (range 0% to 50% in the strait and 8% to 54% in the sound, excluding aquaculture samples). They were present at only one site in northern Puget Trough (see Fig. 1, Table 1).

This Puget Sound and Trough distribution of M. galloprovincialis is largely consistent with that found by Anderson et al. (2002), who sampled similar locations. Differences are that I found M. galloprovincialis alleles at Steilacoom and Elliott Bay Marinas where they did not, but not at Seattle (Harbor Island Marina) or Tacoma (Ole and Charlie's Marina), where they did. I take these minor differences between studies to indicate local spatial heterogeneity in mussel species distributions; with larger sample sizes at identical sites the results would likely be consistent.

The frequency of M. galloprovincialis genes (22%) exceeds previous estimates for Puget Sound by approximately 4-fold (Brooks 1991, Suchanek et al. 1997, Anderson et al. 2002, cultured mussels excluded from all studies). Because my collections and those of Anderson et al. (2002) were made in the same year, the difference does not reflect a temporal change. Instead, I suggest that it may reflect differences in the size of sampled mussels. The subtidal mussels I collected were 3-10 cm in shell length, whereas those analyzed by Anderson et al. (2002) were as small as 0.5 cm. Further evidence for a difference in sizes is found in the detailed analysis by Anderson et al. (2002) of mussels at one site, where they found that smaller mussels had predominantly M. trossulus alleles and larger ones had predominantly M. galloprovincialis alleles. The potentially larger size of M. galloprovincialis has implications for the invader's fecundity and spread relative to its native sibling species.

Although M. galloprovincialis was readily found at subtidal sites, I found none in intertidal samples from Tatoosh Island. Because M. galloprovincialis is common at other intertidal sites in the Pacific and Atlantic (Sarver & Foltz 1993, Quesada et al. 1995b, Rawson & Hilbish 1995a, Wilhelm & Hilbish 1998), it seems likely that it will also invade this habitat in Washington waters. On the other hand, at one site in Posjet Bay, Russia, McDonald et al. (1991) found exclusively M. trossulus intertidally and exclusively M. galloprovincialis subtidally. Only one intertidal hybrid has been reported from Washington (Suchanek et al. 1997), and further sampling is warranted to determine whether M. galloprovincialis is invading intertidal as well as subtidal habitats.

Oregon and Northern California

On the Oregon coast, M. galloprovincialis alleles have been reported only from Yaquina and Coos Bays (see Table 1). Surveys in northern California (north of Cape Mendocino) repeatedly identify M. galloprovincialis alleles in Crescent City and Humboldt Bay (see Table 1). The central and southern California distribution of M. galloprovincialis is summarized elsewhere (McDonald & Koehn 1988, McDonald et al. 1991, Sarver & Foltz 1993, Suchanek et al. 1997).

Allele Frequencies

For a subset of sites in three Northeast Pacific regions (those sites at which M. galloprovincialis alleles were reported, and genetic markers distinguished heterozygotes from homozygotes), mean genotype frequencies were calculated (Table 2). In each region the observed frequencies differed significantly from Hardy-Weinberg equilibrium in goodness-of-fit tests using the total number of each genotype (see Table 2). These departures from equilibrium reflect an under-representation of M. galloprovincialis alleles, which is consistent both with the early stages of an invader's spread into a native population and with more general observations of heterozygote deficiency in Mytilus populations (Raymond et al. 1997).

Invasion Pathways

It seems likely that M. galloprovincialis has been introduced to the Northeast Pacific through both aquaculture and shipping or boating. Most commercial M. galloprovincialis seed in the region is currently supplied by a single farm in Washington, which originally obtained its stock from California in the 1980s (G. King, Taylor United Shellfish, pers. comm.). These mussels were initially imported because they seemed to be resistant to bivalve disseminated-hemic neoplasia, a disease of unknown pathogenic agent that affects native M. trossulus particularly in culture (Brooks & Elston 1989a, Brooks & Elston 1989b). At the time of import, the genetic identity of the disease-resistant Californian mussels was not recognized (G. King, pers. comm.). The introduction date of M. galloprovincialis to California is unknown, but it has been suggested that historical records of a Mytilus invasion in southern California (Burch 1943-1958, Smith 1944, Coe 1945, 1946) reflect the arrival of M. galloprovincialis (Carlton 1979, Geller 1999). Aquaculture farms currently serve as localized sources of reproductively mature M. galloprovincialis whose larvae presumably disperse as far as currents permit. Additional dispersal within the region may occur from wild populations and via adult mussels transported on boat hulls.

Ship ballast water and ship and boat hulls may also provide a continual supply of organisms, including M. galloprovincialis, to Pacific Northwest waters (Carlton & Geller 1993, Geller et al. 1994, Suchanek et al. 1997). Shipping to the region comes primarily from Asia, where M. galloprovincialis is also introduced (Wilkins et al. 1983, Lee & Morton 1985, Inoue et al. 1995, Inoue et al. 1997, Suchanek et al. 1997, Wonham & Carlton 2004). This pathway may be particularly relevant to M. galloprovincialis populations along the Strait of Juan de Fuca, where Vancouver-bound vessels may deballast (Larson et al. 2003, Levings et al. 2004).

Within the northeast Pacific, no study to date has explicitly been designed to assess the spatial spread of mussels from aquaculture facilities, ports, or marinas. Detailed genetic investigation of possible source populations (i.e., Japan, California, and the Mediterranean) may shed light on the likeliest invasion pathways for M. galloprovincialis to the region (Rawson & Hilbish 1995a, Sanjuan et al. 1997, Quesada et al. 1998). Within the region, sampling a range of mussel sizes and habitats (i.e., intertidal and subtidal; rock and floats) at increasing distances from farms, ports, and marinas could provide a clearer picture of the role of these potential M. galloprovincialis sources. Because the species is now widespread, more ecologically interesting questions concern its success and impacts as an invader (e.g., Hockey & Van Erkom Schurink 1992, Geller 1999, Gilg & Hilbish 2000, Secor et al. 2001).

The combined results reported here identity a major zone of sympatry and hybridization between M. galloprovincialis and M. trossulus in Washington waters, in addition to the well-recognized California zone (McDonald & Koehn 1988, McDonald et al. 1991, Sarver & Foltz 1993, Suchanek et al. 1997). The apparent absence of M. galloprovincialis genes between Yaquina Bay, Oregon, and Cape Flattery, Washington, may reflect the absence of mussel culture and major shipping ports along this stretch of coastline. On the other hand, given coastal currents and shipping traffic (Levings et al. 1998, Larson et al. 2003), and the associated potential for larval release and dispersal, it would not be surprising if further sampling revealed that the Washington and California zones comprised a larger Mytilus-complex hybrid swarm extending along the North American Pacific coast.
TABLE 1.
Mussel Mytilus spp. records on the Pacific coast or North America from
Queen Charlotte Strait, British Columbia, to Humboldt Bay, California.
For each site, proportion of, homozygous M. galloprovincialis alleles,
Mg, homozygous M. trossulus alleles, Mt, and heterozygous hybrids,
Mg x Mt, given. N, number of individuals sampled. Sites in bold are
those with M. galloprovincialis or hybrid individuals; p, genes present
but not quantified; nd, data not provided in original study; -, marker
could not distinguish heterozygotes. Latitude ([degrees]N), longitude
([degrees]W), and sampling date (m/yy) given for intertidal and
subtidal mussel Mytilus spp. collection sites in the present study;
sites indicated with * were sampled during a rapid-assessment survey
for introduced marine species in Puget Sound (Cohen et al. 1998).

Location Site Mg Mg x Mt Mt

British Columbia outer coast
 Vancouver Island
 Coal Harbour 0.00 0.00 1.00
 Ucluelet Harbour 0.00 0.00 1.00
Strait of Georgia & Queen
 Charlotte Strait
 Vancouver Island
 Port Hardy 0.00 0.00 1.00
 Sayward 0.00 0.00 1.00
 Yellow Island 0.00 0.06 0.94
 Union Bay 0.04 0.00 0.96
 French Creek 0.06 0.03 0.91
 Nanaimo 0.03 0.03 0.93
 Chemainus 0.14 0.00 0.86
 Mainland
 Horseshoe Bay 0.00 0.00 1.00
 North Puget Trough
 Bellingham Bay * 0.18 0.09 0.73
 0.00 -- 1.00
Saddlebag Island, Padilla Bay 0.00 0.00 1.00
 Anacortes
 Anacortes 0.00 -- 1.00
 Anacortes City Pier * 0.00 0.00 1.00
San Juan Island
 Argyle Creek 0.00 0.00 1.00
 Eagle Cove 0.00 0.00 1.00
 Friday Harbor Laboratory * 0.00 0.00 1.00
Puget Sound-East Basin
 Whidbey Is. (E)
 Deception Pass Marina 0.00 -- 1.00
 Oak Harbor Crescent Harbor 0.00 -- 1.00
 Penn Cove 0.25 0.10 0.65
 0.00 0.00 1.00
 Holmes Harbor (Honeymoon H.) 0.01 0.02 0.97
 Holmes Harbor (Freeland) 0.00 -- 1.00
 Possession Point 0.00 -- 1.00
Puget Sound-Hood Canal
 Hood Canal 0.00 0.00 1.00
 Lilliwaup 0.00 -- 1.00
 Seal Rock, Brinnon 0.00 -- 1.00
 Potlatch State Park 0.00 -- 1.00
 Twanoh State Park 0.00 -- 1.00
 Belfair State Park 0.00 -- 1.00
Puget Sound-Main Basin
 Whidbey Is. (W)
 Fort Casey p nd nd
 Keystone Ferry 0.00 -- 1.00
 Mutiny Bay 0.00 -- 1.00
 Edmonds
 Edmonds Marina * 0.07 0.20 0.73
 Edmonds 0.19 -- 0.82
 Seattle
 Seahurst County Park 0.19 -- 0.81
 Shilshole Bay 0.12 -- 0.88
 Elliott Bay Marina * 0.00 0.15 0.85
 0.00 -- 1.00
 Seattle Pier 91 0.00 -- 1.00
 West Seattle 0.00 -- 1.00
 Harbor Island Marina * 0.00 0.00 1.00
 Des Moines
 Saltwater State Park 0.04 -- 0.96
 Des Moines Marina * 0.14 0.14 0.71
 Tacoma
 Point Defiance 0.07 -- 0.93
 Ole & Charlie's Marina * 0.00 0.00 1.00
 Manchester
 Manchester p nd nd
 Manchester State Park 0.00 -- 1.00
 Silverdale, Dyes Inlet 0.35 -- 0.65
 0.18 0.67 0.15
 Poulsbo, Liberty Bay 0.00 -- 1.00
 Kingston p nd nd
Puget Sound-South Basin
 Steilacoom Marina * 0.00 0.25 0.75
 0.00 -- 1.00
 Budd Inlet
 Skookum Bay 0.00 0.00 1.00
 Tolmie State Park 0.00 -- 0.00
 Boston Harbor Marina * 0.18 0.09 0.82
 Totten Inlet
 Taylor United Shellfish (c) 1.00 0.00 0.00
 Taylor United Shellfish (n) 0.75 0.25 0.00
 Taylor United Shellfish 1.00 -- 0.00
 Carlyon 0.08 -- 0.92
 Hammersley Inlet
 Shelton Yacht Club * 0.43 0.57 0.50
 Shelton 0.33 -- 0.67
 Kamilche Sea Farms 0.00 0.19 0.81
 Case Inlet
 Grapeview Marina 0.09 -- 0.91
 Joemma Beach State Park 0.02 -- 0.98
 Carr Inlet
 Penrose Point State Park 0.02 -- 0.98
 Purdy 0.04 -- 0.96
Strait of Juan de Fuca
 Vancouver Island
 Sooke Harbour 0.00 0.01 0.99
 Victoria 0.00 0.03 0.97
 Sequim
 John Wayne Marina 0.00 1.00 0.00
 0.00 0.18 0.82
 Washington Harbor 0.00 0.00 1.00
 Van Riper's Marina, Sekiu 0.10 0.00 0.90
 Makah Marina, Neah Bay 0.00 0.08 0.92
 Port of Port Angeles 0.23 0.31 0.46
 Tatoosh Island, Cape Flattery 0.17 0.00 0.83
 0.00 0.00 1.00
Washington outer coast
 Ruby Beach 0.00 0.00 1.00
 Westport, Grays Harbor 0.00 0.00 1.00
 Willapa Bay
 Bay Center 0.00 0.00 1.00
 Port of Willapa 0.00 0.00 1.00
 Columbia River 0.00 0.00 1.00
 Oregon coast
 Tillamook Bay 0.00 0.00 1.00
 0.00 0.00 1.00
 0.00 0.00 1.00

 Yaquina Bay
 Yaquina Bay 0.00 0.11 0.89
 0.00 0.00 1.00
 Newport 0.00 0.00 1.00

 0.00 0.00 1.00
 Alsea Bay 0.00 0.00 1.00
 Umpqua River 0.00 0.00 1.00
 Coos Bay 0.09 0.00 0.91
 Port Orford 0.00 0.00 1.00
 0.00 0.00 1.00
California coast
 Crescent City 0.00 p? p
 0.06 0.00 0.94
 p nd nd
 0.04 0.04 0.92
 0.00 0.00 1.00
 Humboldt Bay
 Humboldt Bay 0.88 0.08 0.04
 p nd nd
 Arcata Bay 0.00 0.00 1.00
 0.01 0.01 0.98
 Eureka 0.00 0.00 1.00
 Eureka Slough 0.00 0.01 0.99
 Woodley Island 0.00 0.00 1.00

Location Site N Source

British Columbia outer coast
 Vancouver Island
 Coal Harbour 22 Heath et al. 1995 (a)
 Ucluelet Harbour 23 Heath et al. 1995
Strait of Georgia & Queen
 Charlotte Strait
 Vancouver Island
 Port Hardy 29 Heath et al. 1995
 Sayward 35 Heath et al. 1995
 Yellow Island 79 Heath et al. 1995
 Union Bay 26 Heath et al. 1995
 French Creek 35 Heath et al. 1995
 Nanaimo 29 Heath et al. 1995
 Chemainus 29 Heath et al. 1995
 Mainland
 Horseshoe Bay 25 Heath et al. 1995
 North Puget Trough
 Bellingham Bay * 11 Present study (9/98)
 (48[degrees]76',
 122[degrees]49')
 22 Anderson et al. 2002 (c)
Saddlebag Island, Padilla Bay 1 Present study (7/97)
 (48[degrees]32',
 123[degrees]33')
 Anacortes
 Anacortes 32 Anderson et al. 2002
 Anacortes City Pier * 10 Present study (9/98)
 (48[degrees]31',
 122[degrees]36')
San Juan Island
 Argyle Creek 6 Suchanek et al. 1997
 Eagle Cove 6 Suchanek et al. 1997
 Friday Harbor Laboratory * 2 Present study (9/98)
 (48[degrees]32',
 123[degrees]01')
Puget Sound-East Basin
 Whidbey Is. (E)
 Deception Pass Marina 30 Anderson et al. 2002
 Oak Harbor Crescent Harbor 32 Anderson et al. 2002
 Penn Cove 20 Suchanek et al. 1997
 563 Brooks 1991 (d)
 Holmes Harbor (Honeymoon H.) 200 Brooks 200
 Holmes Harbor (Freeland) 30 Anderson et al. 2002
 Possession Point 28 Anderson et al. 2002
Puget Sound-Hood Canal
 Hood Canal 54 Brooks 1991
 Lilliwaup 30 Anderson et al. 2002
 Seal Rock, Brinnon 54 Anderson et al. 2002
 Potlatch State Park 30 Anderson et al. 2002
 Twanoh State Park 32 Anderson et al. 2002
 Belfair State Park 26 Anderson et al. 2002
Puget Sound-Main Basin
 Whidbey Is. (W)
 Fort Casey nd Brooks 2000
 Keystone Ferry 32 Anderson et al. 2002
 Mutiny Bay 30 Anderson et al. 2002
 Edmonds
 Edmonds Marina * 15 Present study (9/98)
 (47[degrees]49',
 122[degrees]23')
 Edmonds 26 Anderson et al. 2002
 Seattle
 Seahurst County Park 32 Anderson et al. 2002
 Shilshole Bay 68 Anderson et al. 2002
 Elliott Bay Marina * 13 Present study (9/98)
 (47[degrees]38',
 122[degrees]22')
 66 Anderson et al. 2002
 Seattle Pier 91 29 Anderson et al. 2002
 West Seattle 24 Anderson et al. 2002
 Harbor Island Marina * 13 Present study (9/98)
 (47[degrees]35',
 122[degrees]22')
 Des Moines
 Saltwater State Park 28 Anderson et al. 2002
 Des Moines Marina * 14 Present study (9/98)
 (47[degrees]24',
 122[degrees]19')
 Tacoma
 Point Defiance 28 Anderson et al. 2002
 Ole & Charlie's Marina * 9 Present study (9/98)
 (47[degrees]12',
 122[degrees]29')
 Manchester
 Manchester nd Brooks 2000
 Manchester State Park 48 Anderson et al. 2002
 Silverdale, Dyes Inlet 126 Anderson et al. 2002
 54 Brooks 1991
 Poulsbo, Liberty Bay 32 Anderson et al. 2002
 Kingston nd Brooks 2000
Puget Sound-South Basin
 Steilacoom Marina * 12 Present study (9/98)
 (47[degrees]10',
 122[degrees]36'
 62 Anderson et al. 2002
 Budd Inlet
 Skookum Bay 7 Suchanek et al. 1997
 Tolmie State Park 44 Anderson et al. 2002
 Boston Harbor Marina * 11 Present study (9/98)
 (47[degrees]08',
 122[degrees]54')
 Totten Inlet
 Taylor United Shellfish (c) 32 Present study (7/97)
 (48[degrees]13',
 123[degrees]06')
 Taylor United Shellfish (n) 4 Present study (7/97)
 Taylor United Shellfish 58 Anderson et al. 2002
 Carlyon 26 Anderson et al. 2002
 Hammersley Inlet
 Shelton Yacht Club * 14 Present Study (9/98)
 (47[degrees]13',
 122[degrees]05')
 Shelton 26 Anderson et al. 2002
 Kamilche Sea Farms 63 Brooks 1991
 Case Inlet
 Grapeview Marina 32 Anderson et al. 2002
 Joemma Beach State Park 58 Anderson et al. 2002
 Carr Inlet
 Penrose Point State Park 60 Anderson et al. 2002
 Purdy 52 Anderson et al. 2002
Strait of Juan de Fuca
 Vancouver Island
 Sooke Harbour 73 Heath et al. 1995
 Victoria 30 Heath et al. 1995
 Sequim
 John Wayne Marina 9 Brooks 1991
 11 Present study (10/98)
 (48[degrees]04',
 123[degrees]06')
 Washington Harbor 63 Brooks 1991
 Van Riper's Marina, Sekiu 10 Present study (10/98)
 (48[degrees]16',
 124[degrees]18')
 Makah Marina, Neah Bay 13 Present study (10/98)
 (48[degrees]22',
 124[degrees]37')
 Port of Port Angeles 13 Present study (10/98)
 (48[degrees]07',
 123[degrees]26')
 Tatoosh Island, Cape Flattery 6 Suchanek et al. 1997
 92 Present study (6/00)
 (48[degrees]23',
 124[degrees]44')
Washington outer coast
 Ruby Beach 72 Brooks 1991
 Westport, Grays Harbor 63 Brooks 1991
 Willapa Bay
 Bay Center 81 Brooks 1991
 Port of Willapa 54 Brooks 1991
 Columbia River 54 Brooks 1991
 Oregon coast
 Tillamook Bay 25 McDonald and Koehn 1988
 (e)
 121 McDonald and Siebenaller
 1989
 17 Suchanek et al. 1997

 Yaquina Bay
 Yaquina Bay 54 Brooks 1991
 338 McDonald and Siebenaller
 1989
 Newport 25 McDonald and Koehn 1988

 68 Rawson and Hilbish 1995
 Alsea Bay 144 McDonald and Siebenaller
 1989
 Umpqua River 111 McDonald and Siebenaller
 1989
 Coos Bay 43 Suchanek et al. 1997
 Port Orford 25 McDonald and Koehn 1988
 30 Rawson and Hilbish 1995
California coast
 Crescent City 21 McDonald and Koehn 1988
 84 Rawson et al. 1999
 [greater Sarver and Loudenslager
 than or 1991
 equal
 to] 32
 48 Salver and Foltz 1993
 29 Rawson and Hilbish 1995
 Humboldt Bay
 Humboldt Bay 98 Brooks 1991
 [greater Sarver and Loudenslager
 than or 1991
 equal
 to] 59
 Arcata Bay 34 Rawson and Hilbish 1995
 83 Rawson et al. 1999
 Eureka 25 McDonald and Koehn 1988
 Eureka Slough 192 Sarver and Foltz 1993
 Woodley Island 60 Sarver and Foltz 1993

Notes:

(a) ITS alleles only. This marker did not distinguish M.
galloprovincialis from the introduced Atlantic M. edulis, so samples
listed here under M. galloprovincialis may have included both.

(b) Mussels in present study selected for large size (all 3-10 cm
shell length).

(c) Mussels in Brooks (1991) selected for M. galloprovincialis-type
morphologies.

(d) In Anderson et al. (2002), hybrids were not distinguished from
individuals with only M. galloprovincialis alleles.

(e) Mpi alleles only.

TABLE 2.
Mean ([+ or -] SD) for homozygote and heterozygote Mytilus allele
frequencies in 3 regions of the northeast Pacific from Table 1
(number of sites per region in parentheses). Allele frequencies
in all 3 regions for Mg, homozygous M. galloprovincialis, Mt,
homozygous M. trossulus, and Mg x Mt, heterozygous hybrids, are
significantly different from Hardy-Weinberg equilibrium at p
< 0.0001, based on contingency table tests using the number of
mussels of each genotype.

 Site Mg Mg x Mt

Puget Sound (11) 0.18 (0.23) 0.24 (0.20)
Strait of Juan de Puca (8) 0.06 (0.09) 0.20 (0.34)
Oregon & California (7) 0.15 (0.32) 0.04 (0.04)

 Site Mt [chi square]

Puget Sound (11) 0.63 (0.30) 228.9
Strait of Juan de Puca (8) 0.74 (0.34) 136.5
Oregon & California (7) 0.81 (0.34) 495.3


ACKNOWLEDGMENTS

Many thanks to J. Mitton and B. Kreiser at the University of Colorado, Boulder, and S. Edwards at the University of Washington, Seattle, for making laboratory space, equipment, and reference samples available. K. Ward provided expert laboratory assistance, and K. Brooks and two anonymous reviewers provided valuable comments. G. King arid Taylor Shellfish Inc. generously made mussel samples available. This work was supported by Graduate Research Fellowship NA77OR0250, Estuarine Reserves Division, Office of Ocean and Coastal Management, National Ocean Service, National Oceanic and Atmospheric Administration (Padilla Bay National Estuarine Research Reserve). Access to Tatoosh Island was permitted by the Makah Tribal Council.

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MARJORIE J. WONHAM *

University of Washington, Department of Zoology, Box 351800, Seattle, WA, USA 98195-1800

* Corresponding author. E-mail: mwonham@ualberta.ca
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