The relationship between allele frequency and tidal height in a mussel hybrid zone: a test of the differential settlement hypothesis

The blue mussels Mytilus edulis L. and M. galloprovincialis Lmk. hybridize in western Europe. Within hybrid populations nuclear alleles specific to M. galloprovincialis increase in frequency with age and size. This relationship changes with tidal height; alleles from M. galloprovincialis occur more frequently high in the intertidal zone, while M. edulis alleles predominate in the low intertidal zone. We tested the hypotheses that larvae with M. galloprovincialis alleles tend to settle higher in the intertidal zone, or that mussels redistribute themselves with respect to tidal height after initial larval settlement. We sampled recently metamorphosed mussels every 2 weeks in a hybrid mussel population at Whitsand Bay in southwest England throughout the summer of 1996. We observed four cohorts of newly settled mussels. There was no evidence of differential settlement of mussels with different genotypes in connection with tidal height, or into shaded versus unshaded microsites. Therefore, we rejected the preferential settlement hypothesis. There was substantial movement of juvenile mussels in the first 4 weeks following initial settlement, but this “secondary settlement” did not result in genetic differentiation with respect to tidal height. Further, significant differences in allele frequencies were found between primary and secondary spat. This allele frequency change was in the opposite direction of that seen in the adult population, suggesting newly settled larvae may be experiencing different selective pressures than adults. We propose that the genetic structure of hybrid mussel populations with respect to tidal height is the consequence of differences in selection intensity. Received: 30 April 1999 / Accepted: 5 May 2000     

Implications of movement behavior on mussel dislodgement: exogenous selection in a<Emphasis Type="Italic"> Mytilus</Emphasis> spp. hybrid zone

Rocky intertidal habitats often exhibit high levels of environmental heterogeneity, and the ability of organisms to move between microhabitats is likely to have a profound influence on their rates of mortality and overall fitness. Mussels within the Mytilus edulis complex are morphologically very similar, yet at sites where these species hybridize in southwest England, populations repeatedly show evidence of selection against individuals with alleles specific to M. edulis Linnaeus, in favor of those with alleles specific to M. galloprovincialis Lamarck. Differential movement rates of these two species were examined within simulated mussel beds (gravel substrate) in the winter (February) and summer (July) of 2001. M. edulis-like mussels moved more frequently and more quickly to the exterior of gravel beds than did M. galloprovincialis-like mussels. Coupled with measurements of attachment strength in the field conducted in July 2001, we used a wave force model to examine the probability of dislodgement for each species under a range of water velocities. Results suggest that by preferentially moving to the exterior of beds, M. edulis experiences higher dislodgement rates due to exposure to large hydrodynamic forces than do M. galloprovincialis. As a consequence of lower attachment strengths, M. edulis is also predicted to have higher mortality rates than M. galloprovincialis in interior portions of the bed. Thus, differential movement behavior may contribute to the differential genotype-specific mortality rates observed in the Mytilus spp. hybrid zone in southwest England, and is an example of behavior potentially modifying rates of exogenous selection in an intertidal hybrid zone.Communicated by J.P. Grassle, New Brunswick     

Genetic structure of hybrid mussel populations in the west of Ireland: two hypotheses revisited

In Ireland, mussels on exposed rocky shores constitute an interbreeding mixture of two forms of mussels, the blue mussel, Mytilus edulis, and the Mediterranean mussel, M. galloprovincialis. Results from an Irish study in the 1980s, using partially diagnostic allozyme markers, indicated that mussels higher up the shore were more galloprovincialis-like than those lower down. In this study we set out to test two hypotheses: (a) recruits arriving on the shore are composed of genetically distinct cohorts that settle preferentially at different levels on the shore, and maintain genetic distinctiveness into adulthood; (b) recruits are genetically homogeneous, but once settled they diverge genetically over time, due to within-habitat site specific-selection. The diagnostic Me 15/16 DNA marker was used to analyse the genetic composition of newly-settled spat recruiting to artificial substrates, which were placed at two-week intervals from May–October 2002, on the mid- and low shore areas of two exposed sites in Galway Bay. Adult mussels were also collected on each sampling date. Results did not support the preferential settlement hypothesis, i.e., the genetic composition of primary settlers (≤ 500 μm) was similar between tidal heights and shores. Neither was there evidence of post settlement selective mortality, as adults were genetically similar to settling spat. In spat and adults the frequency of the M. galloprovincialis allele was high (0.56–0.80), due to high frequencies of M. galloprovincialis (> 37%) and hybrid (> 33%) genotypes, and correspondingly low frequencies of the M. edulis genotype (< 11%). Adult mussels from a nearby sheltered estuarine site, while significantly different to exposed shore mussels, still had low frequencies of the M. edulis genotype (< 17%), indicating no apparent advantage for the genotype in this environment. There are indications that the genetic composition of mussels may be changing on the Atlantic coasts of Ireland.     

Genetic variation of mitochondrial DNA in mussel (Mytilus edulis and M. galloprovincialis) populations from South West England and South Wales

Mitochondrial DNA (mtDNA) and allozyme variation were analysed in samples of mussels collected in 1984 and 1985 from four localities in South West England and one locality in South Wales, a region of Britain where the common mussel (Mytilus edulis) occurs sympatrically and hybridises with the Mediterranean mussel (M. galloprovincialis). Significant differences in mtDNA genotype frequencies for three restriction enzymes (BstEII, XbaI, and EcoRI) were observed between mussels from M. galloprovincialis populations (Padstow and Bude) and those from an M. edulis population (Swansea). Some mtDNA genotypes at high-frequency in M. galloprovincialis were not observed in M. edulis, although there was no indication that mtDNA variation provides greater overall diagnostic power than allozyme variation in distinguishing between the two forms of mussel. Construction of a phylogenetic tree of multiple mtDNA genotypes revealed small mutational distances between the genotypes characterising M. edulis and M. galloprovincialis. The results were consistent with predominant mtDNA flow from M. edulis to M. galloprovincialis. This can be explained by the dispersal of larvae to South West England from M. edulis regions to the north and east, but little dispersal in the opposite directions. Samples from two hybrid populations (Whitsand and Croyde) were analysed. mtDNA genotype frequencies at Croyde were in line with predictions made on the basis of two partially diagnostic allozyme loci (Est-D and Odh), mtDNA frequencies at Whitsand were not. Frequencies of some mtDNA genotypes at Whitsand were characteristic of M. edulis, others of M. galloprovincialis. Differential selective mortality or flow of different mtDNA genotypes and allozyme variation are proposed as possible causes of these results.     

Hybridization between the blue mussels Mytilus galloprovincialis and M. trossulus along the Pacific coast of North America: evidence for limited introgression

Two species of blue mussel, Mytilus galloprovincialis and M. trossulus, co-occur and hybridize along the Pacific coast of North America. Using a set of polymerase chain-reaction (PCR)-based genetic markers which diagnostically identify these species, we show that they are sympatric from the Cape Mendocino region to the Monterey Peninsula in northern and central California, USA. Mussels with hybrid genotypes were detected in all populations sampled in the region of sympatry, and the frequency of hybrid genotypes in individual hybrid populations ranged from 13 to 44%. Significant frequencies of first-generation backcross genotypes were detected in two individual hybrid zone populations (Berkeley and Monterey Marina) and in the hybrid zone as a whole, indicating that the potential exists for introgression between M. galloprovincialis and M. trossulus. Despite this potential, we found no evidence of advanced introgression beyond first-generation backcrosses, suggesting that gene flow between M. galloprovincialis and M. trossulus has been quite limited. The frequency of mussels with M. trossulus and hybrid genotypes declined abruptly south of Monterey Peninsula, while the frequency of mussels with M. galloprovincialis and hybrid genotypes declined precipitously north of Cape Mendocino. These abrupt genetic discontinuities indicate that this blue mussel hybrid zone is presently positioned between two prominent coastal features and there is little, if any, export of alleles from the hybrid zone into bordering parental populations. Received: 20 August 1997 / Accepted: 26 October 1998     

Genotype-dependent fecundity and temporal variation of spawning in hybrid mussel (Mytilus) populations

Mussel samples were collected at 4 to 6 wk intervals throughout 1987 from two hybridMytilus edulis/M. galloprovincialis populations, at Croyde Bay and Whitsand Bay, in southwest England. These were analyzed at two polymorphic loci which are diagnostic for allozyme differences which typifyM. edulis andM. galloprovincialis. Dry mantle weight as a function of shell length was determined for all individuals of each sample. Size-frequency data for the two populations was obtained in September 1987 and March 1988. For all genotypes at both sites, fecundity was a function of shell length, and in both populations the frequency ofM. galloprovincialis alleles was positively correlated with shell length. At both sites, allozyme genotype explained a significant amount of variation in mantle weight either when assessed as a main effect or when assessed as an interaction with shell length or time of collection. At Croyde,M. galloprovincialis mussels had greater estimated fecundity per unit length than theM. edulis mussels. Differences in the timing of spawning activity between theM. edulis and theM. galloprovincialis mussels were inferred, and these differences might act to reduce the amount of interbreeding at Croyde. At Whitsand, a reduced level of variability in the timing of spawning activity and fecundity between the genotypes was observed and explained by a higher degree of genetic mixing. Because theM. galloprovincialis mussels had (1) a greater estimated fecundity at any length, and (2) a greater mean length than theM. edulis mussels, the mean genotypic annual fecundity perM. galloprovincialis mussel was 2.8 times greater than an individualM. edulis mussel at Croyde, and 2.2 times greater than an individualM. edulis mussel at Whitsand. This evidence thatM. galloprovincialis mussels have an advantage in fecundity, and thus perhaps in fertility, taken together with the evidence thatM. galloprovincialis also has a higher viability, indicates directional selection in favour of theM. galloprovincialis phenotype. Because of the observed temporal stability of the population it seems likely that this selection is counterbalanced by a massive imigration ofM. edulis spat from neighbouring populations.     

Heterozygosity and growth in transplanted mussels

Growth comparisons were made involving mussels (Mytilus spp.) collected from five different localities in Britain in 1980–1981. Two of the localities, Mumbles, South Wales, and Bude, Southwest England, have pure populations of M. edulis and M. galloprovincialis, respectively. The other three, Whitsand Bay, Southwest England, Croyde Bay, Southwest England and Robin Hood's Bay, Northeast England, have hybrid populations with both M. edulis and M. galloprovincialis ancestry. To make growth comparisons, mussels from different populations were mixed in oyster nets and transplanted to three different localities. After periods of transplantation varying between several months and one year, growth was assessed by measuring increase in shell length or dry body weight. Starch-gel electrophoresis was used to assay variation in the transplanted mussels at three allozyme loci partially diagnostic for M. edulis and M. galloprovincialis. The results provide evidence of small growth differences between populations and between allozyme genotypes within populations. These differences accounted for no more than a few percent of the total variation in growth between mussels. Statistically significant results were obtained, but were frequently found not to be reproducible. There is no clear evidence of a growth difference between M. edulis and M. galloprovincialis. Allozyme heterozygotes appear to have growth rates intermediate between allozyme homozygotes; this study thus fails to provide evidence for overdominance with respect to growth rate.     

Factors influencing differential mortality within a marine mussel (Mytilus spp.) hybrid population in southwestern England: reproductive effort and parasitism

Two species of marine mussel, Mytilus edulis and M. galloprovincialis hybridize on the coasts of western Europe. Studies of hybrid mussel populations have shown that natural selection favors M. galloprovincialis-like genotypes within this hybrid zone. Many hypotheses have been proposed to explain differential mortality in these populations. This study tests two hypotheses addressing factors of mortality in a population, and describes yearly energy storage and reproductive cycles of these two species and their hybrids. No evidence was found that the two taxa have different overall levels of reproductive effort or parasite infestation. They do, however, have asynchronous spawning periods and divergent energy storage strategies. In the year of this study, 1993, the M. edulis genotypic class spawned as a group in June and July. After spawning, they built up a high level of mantle energy-storage tissues that are probably used for gametogenesis in the following winter and spring. The M. galloprovincialis genotypic group, however, spawned asynchronously, beginning in June and finishing by August, and did not build up high levels of energy-storage tissues in summer. These results add a temporal component to the interpretation of selective forces acting to shape this hybrid zone. Vulnerability of each species to mortality factors may differ because of their divergent reproductive and energy-storage cycles. Received: 15 January 1999 / Accepted: 26 July 2000     

Growth and survival differences among native,introduced and hybrid blue mussels (<Emphasis Type="Italic">Mytilus</Emphasis> spp.): genotype,environment and interaction effects

The Mytilus species complex consists of three closely related mussel species: Mytilus trossulus, Mytilus edulis, and Mytilus galloprovincialis, which are found globally in temperate intertidal waters. Introduction of one or more of these species have occurred world-wide via shipping and aquaculture. Stable hybrid zones have developed in areas where these species have come into contact, making the invasion process complex. On the east coast of Vancouver Island (VI), British Columbia (BC), Canada, the native (M. trossulus) and introduced species (M. edulis and M. galloprovincialis), as well as their hybrid offspring, occur sympatrically. This study used a common environment experiment to quantify growth and survival differences among native, introduced, and introgressed mussels on VI. Mussels were collected from an area of known hybridization and reared in cages from May to August 2006. The cages were deployed at a local site as well as a remote site (approximately 150 km apart), and the mussels were genotyped at two species-specific loci. Growth and survival, as fitness measures, were monitored: native, introduced, and introgressed individuals were compared between and within sites to determine whether growth and survival were independent of site and genotype. Overall, mussels reared at Quadra Island performed better than locally-reared mussels at Ladysmith. Specifically, introgressed mussels reared at Quadra Island performed better than all genotypes reared at Ladysmith, as well as better than native mussels reared at Quadra Island. Differences in survival and growth among the native, introduced and introgressed mussels may serve to explain the complex hybridization patterns and dynamics characteristic of the VI introgression zone.     

Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis, M. trossulus) and their hybrids from Newfoundland

The mussels Mytilus edulis L. and M. trossulus Gould are found sympatrically in most areas of Newfoundland, with a low frequency of hybrids. To assess the potential for reproductive isolation, we sampled mussels from three sites in an eastern Newfoundland Bay from May–October 1996 to determine if there were differences in the reproductive cycles of the two species and their natural hybrids. In mussels with sheil lengths of 38–42 mm, males and females with mature gametes were dominant in June for M. edulis and hybrids, while M. trossulus showed a lower frequency of individuals with mature gametes. M. trossulus and hybrids spawned over a prolonged period (from late spring to early autumn) compared with most M. edulis individuals that spawned over a period of 2–3 weeks in July. This asynchrony in spawning activity between the two species may partially explain the low frequency of hybrids found in previous studies of these mussel populations. Female and male hybrids between M. edulis and M. trossulus showed normal gonad development, ripening and spawning, providing an opportunity for the introgression of genes between the two species. M. trossulus had a higher reproductive output than M. edulis of similar shell length, while hybrids showed intermediate values of reproductive output. M. trossulus females produced smaller eggs than either M. edulis or hybrids. Differences in reproductive traits may partially explain the maintenance of the mussel hybrid zone in Newfoundland. Published online: 13 August 2002     

Spatio-temporal patterns in the genetic structure of recently settled blue mussels (<Emphasis Type="Italic">Mytilus</Emphasis> spp.) across a hybrid zone

Previous studies of a hybrid zone between the mussels Mytilus edulis Linnaeus and M. galloprovincialis Lamarck have not resolved the relative importance of the genetic composition of settling larval cohorts versus post-settlement selection in determining the distribution of the parental species and their hybrids. In the present study, recently settled mussels (spat) were collected from 20 sites in southwest England throughout the summer and fall (May–October) in 1998 and 1999. This study investigated the spatio-temporal patterns of settlement and genetics of mussel spat by genetically identifying M. edulis, M. galloprovincialis and their hybrids using the diagnostic PCR marker Glu-5. Settlement was observed earlier in populations of M. edulis than in populations of M. galloprovincialis. Settlement occurred in hybrid populations at times intermediate to and overlapping with both of the parental populations. Temporal genetic variation within years was rare at most sites, while there was some variation between the two years. Spatial genetic variation, however, was common among spat settling within the hybrid populations and matched that observed in small, sub-adults at the same sites. No consistent directional changes in allele frequency were observed over the course of several weeks after settlement. These data suggest that the observed spatial variation in the adult populations is the result of spatial variation in settling larval cohorts and not of either temporal genetic variation or of selection soon after settlement.Communicated by J.P. Grassle, New Brunswick     

Variation in strength of attachment to the substrate explains differential mortality in hybrid mussel (Mytilus galloprovincialis and M. edulis) populations

Mussel samples were collected from a hybrid mussel (Mytilus galloprovincialis and M. edulis) Population at Croyde, southwest England, in January, March and May 1990. The strength of attachment of each mussel to the substrate was measured with a spring balance. A number of diagnostic characters were also recorded. These are shell lengh, width and height, mantle colour and genotype at two allozyme loci, esterase-D and octopine dehydrogenase. Multiple-regression analysis was used to assess the effect of the diagnostic characters on strength of attachment as dependent variable. Mussels possessing the relatively high shells and darker mantle colouration characteristic of M. galloprovincialis had higher values, on average, for strength of attachment than mussels resembling M. edulis. Phenotypically intermediate mussels had intermediate values for strength of attachment. The results suggest an adaptive difference which can account for reports of differential mortality acting in favour of M. galloprovincialiis.     

Introgression and mitochondrial DNA heteroplasmy in the Baltic populations of mussels Mytilus trossulus and M. edulis

A strong clinal change in salinity occurs between the Baltic Sea and the North Sea, Atlantic Ocean, in the Danish Straits, where hybridization zone between mussels Mytilus edulis and M. trossulus has been reported. Eleven samples of mussels were studied from the Danish Straits and the inner Baltic Sea. Extensive introgression of M. edulis alleles from the North Sea into populations throughout the Baltic was ascertained for mitochondrial DNA (mtDNA) and two nuclear markers (ME15–16 and ITS). In the opposite direction, introgression of M. trossulus alleles into the M. edulis background was observed at the EFbis nuclear marker in populations from Kattegat (Danish Straits). While only M. edulis F (female) mtDNA was present in the Baltic, there were still strong differences in frequencies in the control region length variants between the Danish Straits and the inner Baltic samples, and weaker variation in coding region ND2–COIII haplotype frequencies. In the assays of the two mtDNA regions, various patterns of heteroplasmy were detected in 32% of all the studied individual mussels; this includes the presence of distinct, independently inherited M and F mitochondria in males, as well as the presence of two different distinguishable F genomes. The male-inherited M mtDNA genomes are quite common in the mussels from the Danish Straits, but very rare in males from the inner Baltic. Instead, a recombined control region variant (1r), which seems to have taken over the role of the M genome, was present in a number of specimens in the Baltic. Observations of heteroplasmy for two F genomes in some females and males confirm disruptions of the doubly uniparental inheritance mechanism in the hybrid Baltic Mytilus.     

The Mytilus edulis species complex in southwest England: effects of hybridization and introgression upon interlocus associations and morphometric variation

Loglinear analysis of electrophoretic data from two hybrid Mytilus edulis x galloprovincialis populations in southwest England revealed non-significant associations between genotypes at four allozyme loci, each of which is partially diagnostic for differences between the two taxa. Significant non-random genotypic associations within the context of the non-significant model involved all four assayed loci equally, consistent with their occurrence in a relatively tight linkage group. Multivariate analyses were used to examine electrophoretic variation from the two hybrid populations, and morphometric variation in the hybrid populations and in four allopatric (two M. edulis and two M. galloprovincialis) populations from western Europe While the number of hybrid mussels is high at both sites (22% at Croyde, 53% at Whitsand) the two taxa have largely maintained the genetic differences which exist between them in allopatry. However, morphological differences between the taxa have been eroded for mussels within the hybrid zone, whereas these differences are quite pronounced for mussels from allopatric populations. It is proposed that each taxon within the genus maintains its genetic identity, despite high dispersal potential, widespread hybridization, and high levels of introgression, as a result of adaptation to different environments. The worlwide occurrence of all four Mytilus hybrid zones at ecotones between recognized biogeographical provinces which are characterized by differences in temperature and salinity is consistent with such an interpretation.     

Size-dependent, spatial and temporal genetic variation at a leucine aminopeptidase (LAP) locus among blue mussel (Mytilus galloprovincialis) populations along a salinity gradient

Biochemical genetic variation at a leucine aminopeptidase (LAP) locus is related to salinity variation in several marine bivalve molluscs. This paper details an investigation of the Long Island Sound model of LAP selection (LAP genotype-dependent mortality occurring among newly settled Mytilus edulis mussels) carried out in 1997 among three M. galloprovincialis mussel populations along the salinity gradient of Wellington Harbour, New Zealand. Significant LAP genotypic heterogeneity was observed at the LAP locus between small (<25 mm shell length) and large (>25 mm shell length) M. galloprovincialis from Petone and Eastbourne (the two sites experiencing the greatest salinity variation), whereas genotypic heterogeneity was not significantly different between small and large mussels from Seatoun (the site experiencing the least salinity variation). The Lap ³ allele decreased in frequency and the Lap ⁴ allele increased in frequency at Petone and Eastbourne, whereas the Lap ³ and Lap ⁴ allele frequencies remained effectively constant at Seatoun. Both these findings are consistent with the Long Island Sound model of selection. At all three locations, the Lap ^3,3 genotype decreased in frequency from small to large mussels, whereas the Lap ^3,4 genotype increased in frequency from small to large mussels. All other LAP genotypes occurred at low frequencies (<0.10) at all three locations and showed no evidence of frequency change from small to large-size mussels nor evidence of clinal change among the three locations. These genotype frequency data possibly indicate that the Lap ^3,3 genotype is at a selective disadvantage compared to the Lap ^3,4 genotype at all three locations, and that this selective disadvantage is related to the extent of salinity variation which exists at each location. Further investigation is required before it can be determined if the Long Island Sound model of selection best describes the size-dependent and location-specific changes in LAP allele and genotype frequencies along this salinity gradient. Comparison of the population genetic structure at the LAP locus in 1995 and in 1997 revealed a profound change from heterozygote excesses to heterozygote deficiencies for all three M. galloprovincialis populations. The reason for the change is unknown, but the change indicates that population genetic structure at the LAP locus is highly variable in time, but consistent in space, among these M.␣galloprovincialis populations. Received: 5 February 1998 / Accepted: 27 May 1998     

Genetic characterization of the hybridization betweenMytilus edulis andM. galloprovincialis on the Atlantic coast of France

A genetic study carried out on nine natural mussel populations on the French Atlantic coast from 1989–1990 revealed interdigitation between typicallyMytilus edulis and typicallyM. galloprovincialis populations and intermediate populations. The allele components of the populations followed aM. edulis/M. galloprovincialis gradient which does not correspond to a geographical gradient. Strong hybridization was evident in samples with intermediate allele frequencies. The respective importance of gene flow and selection is discussed in the light of the results and the evironmental features of the sampling zone.     

Distribution of Mytilus edulis, M. galloprovincialis, and their hybrids in open-coast populations of mussels in southwestern England

The distribution of Mytilus edulis Linnaeus, M. galloprovincialis Lamarck, and their hybrids was examined in mussel populations in southwest England in 1996 and 1998. This is a region where both parental taxa and populations containing large numbers of hybrids co-occur yet a fine-scale mapping of the hybrid populations has not been conducted. In this study the geographic distribution of hybrid populations was determined in southwest England over 360 km of coast from Tintagel Castle in north Cornwall to Beer in south Devon. Sample localities were spaced from 5 to 20 km apart. Genotypes for individual mussels were determined using PCR to amplify a size polymorphism at the Glu-5' locus that is completely differentiated between M. edulis and M. galloprovincialis. Hybrid populations, characterized by high frequencies of individuals with heterozygous genotypes and a pattern of decreasing frequency of M. edulis alleles with increasing shell length, were continuously distributed along 180 km of open coast in southwest England. This "hybrid patch" was bordered at one end by geographically extensive populations of pure M. edulis and at the other end by nearly pure populations of M. galloprovincialis. Strong natural selection in hybrid populations results in a decline in the frequency of M. edulis alleles with increasing size. Wave-exposure has previously been implicated as the agent producing this pattern of selection, but in the present study the relationship between allele frequency and body size was not correlated with variation in wave shock intensity among localities within the hybrid zone. The transition between hybrid populations and those containing pure populations of M. edulis or M. galloprovincialis is abrupt which suggests that coastal circulation patterns may provide strong barriers to larval dispersal which accounts for the position and maintenance of the hybrid zone.     

Wave action and competitive interaction between the invasive mussel Mytilus galloprovincialis and the indigenous Perna perna in South Africa

On the south coast of South Africa, the invasive alien mussel Mytilus galloprovincialis shows partial habitat segregation with the indigenous mussel Perna perna. P. perna predominates in the lower mussel zone and M. galloprovincialis in the upper zone, with mixed beds where the two overlap. We examined competitive interactions between these species by translocating mussels into small plots at high densities. Treatments involved different combinations of species and densities placed in each zone. Mortality was monitored regularly and at the end of each experiment, growth and condition index were measured. The experiment was attempted three times. The first two attempts were disrupted by wave action, especially winter storms, but provided information on species-specific effects of wave action. In experiment one, wave induced mortality decreased from a mean for both species of approximately 90% on the low shore to ca. 50% on the high shore, and was 15–30% lower for P. perna than M. galloprovincialis in each zone. In experiment two, M. galloprovincialis mortality was not affected by zone (Kruskal–Wallis test, P > 0.05), but was higher than P. perna mortality in the low zone (P < 0.05). P. perna survival was significantly (P < 0.05) lower on the high than mid and low zones, apparently due to the effects of greater emersion. Condition index showed a similar pattern, being lowest in the low zone for M. galloprovincialis and in the high zone for P. perna (3-way ANOVA, P < 0.05). Growth rates were fastest for both species in the low zone (Kruskal–Wallis, P < 0.05 in both cases). The third experiment was run for 12 months in the low zone only and provided evidence of intraspecific competition for P. perna and of interspecific competition. Condition was significantly greater for P. perna in all treatments (2-way ANOVA), as was growth (Kruskal–Wallis P < 0.05). Significant treatment effects indicated that P. perna had a negative effect on M. galloprovincialis survival (Kruskal–Wallis, P < 0.05). Again wave action was important; by the end of the experiment all mussels had been removed from plots stocked only with M. galloprovincialis. Thus P. perna improves survival of M. galloprovincialis on the low shore in the short term, by providing protection against wave action, but excludes it competitively in the longer term. The results show that partial habitat segregation is likely to be a permanent feature on the south coast, with M. galloprovincialis unable to dominate the low shore due to the effects of waves and competitive exclusion by P. perna. This study is the first attempt to examine the mechanisms of interaction between invasive and indigenous marine mussel species and provides evidence of the importance of environmental conditions in the mediation of this interaction.     

Origin of the antitropical distribution pattern in marine mussels (Mytilus spp.): routes and timing of transequatorial migration

Many marine species, including mussels in the Mytilus edulis species group (i.e. M. edulis L., M. galloprovincialis Lamarck, and M. trossulus Gould), have an antitropical distribution pattern, with closely related taxa occurring in high latitudes of the northern and southern hemispheres but being absent from the tropics. We tested four hypotheses to explain the timing and route of transequatorial migration by species with antitropical distributions. These hypotheses yield different predictions for the phylogenetic relationship of southern hemisphere taxa relative to their northern counter-parts. The three Mytilus species were used to test these hypotheses since they exhibit a typical antitropical distribution and representative taxa occur in both the Pacific and Atlantic. Two types of mtDNA lineages were found among populations of mussels collected from the southern hemisphere between 1988 and 1996; over 90% of the mtDNA lineages formed a distinct subclade which, on average, had 1.4% divergence from haplotypes found exclusively in northern Atlantic populations of M. galloprovincialis. These data indicate that southern hemisphere mussels arose from a migration event from the northern hemisphere during the Pleistocene via an Atlantic route. The remainder of the southern hemisphere lineages (<10%) were very closely related to mtDNA haplotypes found in both M. edulis and M. galloprovincialis in the northern hemisphere, suggesting a second, more recent migration to the southern hemisphere. There was no evidence that southern hemisphere mussels arose from Pacific populations of mussels. Received: 8 December 1998 / Accepted: 8 November 1999     

Molecular population genetics of male and female mitochondrial genomes in European mussels <Emphasis Type="Italic">Mytilus</Emphasis>

The doubly uniparental system of mitochondrial inheritance (DUI) is best known in marine mussels Mytilus. Under DUI there are two types of mitochondrial DNA (mtDNA). The female type (F) is transmitted to offspring of both genders and the male type (M) exclusively to sons; consequently two distinct mtDNA lineages exist. The M lineage evolves under more relaxed selection than the F lineage resulting in higher polymorphism within the M lineage. Though this polymorphism is expected to make inferences on fine population structure easier using M instead of F data, no comprehensive comparative data exist to support this claim. We sequenced a 1,205 bp fragment of M and F mtDNA comprising parts of the COIII and ND2 genes, and analysed 204 individuals representing three Mytilus species: M. edulis, M. galloprovincialis and M. trossulus from 13 European sampling sites. A clear distinction between Mediterranean and Atlantic populations was found with both M and F data, but much better geographic differentiation was found within the Atlantic using F rather than M data. In particular, Atlantic M. galloprovincialis can be differentiated from Atlantic M. edulis, and further subdivision of Atlantic M. edulis is possible using the F data but not the M data. Multiple tests of selection were carried out to attempt to explain this paradox. We concluded that the overall pattern of polymorphism is consistent with strong purifying selection; not only is this selection relaxed in the M lineage in comparison with the F lineage, but it is also more frequently interrupted by periodic selective sweeps within the M lineage.