Origin of Fucus Serratus (Heterokontophyta; Fucaceae) Populations in Iceland and the Faroes: a Microsatellite-Based Assessment

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Eur. J. Phycol. (2006), 41(2): 235–246

Origin of Fucus serratus (Heterokontophyta; Fucaceae) populations in Iceland and the Faroes: a microsatellite-based assessment

J. A. COYER1, G. HOARAU1, M. SKAGE2, W. T. STAM1 AND J. L. OLSEN1

1Department of Marine Biology, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands 2Department of Biology, University of Bergen, 5007 Bergen, Norway

(Received 13 October 2005; accepted 22 February 2006)

The common intertidal seaweed Fucus serratus was almost certainly introduced to Iceland and the Faroes by humans from Europe, as previous genetic studies have confirmed that life-history constraints preclude long-distance dispersal. Introduction must have occurred sometime in the 1,000 years between arrival of the first Icelandic settlers c. 900 AD and when the species was first noted in a phycological survey in 1900. We genotyped 19 populations from throughout northern Europe, Iceland, and the Faroes with seven microsatellite loci in order to identify the source or sources of the Icelandic/Faroese populations. Assignment tests indicated that the Sma˚skjaer area of the Oslofjorden in Norway was the source for the Icelandic populations and the Hafnarfjo¨ rôur area of Iceland was the likely source for the single Faroese population. The time of introduction to Iceland was probably during the 19th century, whereas introduction to the Faroes occurred during the late 20th century. Additionally, molecular data verified hybridization between the introduced F. serratus and the native F. evanescens.

Key words: Fucus serratus, hybridization, Iceland, species introductions, seaweeds, the Faroes

Introduction biological surveys in the mid-1800s was largely Recent introductions of marine species due to the a result of post-glaciation colonization, and that it shipping and fisheries activities of human societies was only after the surveys that novel species were continue to be a widely discussed topic. With the noted and attributed to human-induced introduc- heightened awareness of the extent and effect of tions. In reality, however, extensive maritime contemporary introductions, it is easy to forget activities existed along the northeastern Atlantic that marine species have been transported from coast for many centuries before the first biological one area to another, on or in the hulls of wooden surveys, and marine species undoubtedly were ships and their rock or sand ballast, for centuries routinely transported via the wooden hulls, rock or millennia before the first biological surveys ballast, or packing materials. began in the mid-1800s (Carlton, 1999; 2003). Maritime activities between northern Europe Indeed, the long history of species introductions and the central North Atlantic islands (Iceland, facilitated by human maritime activities almost the Faroes, Greenland) effectively began with the certainly has clouded present worldwide views of Norse Vikings in the late 800s. Travel among the coastal marine ecology, biodiversity, and biogeo- islands, and between the islands and Norway, graphy (Carlton, 2000, 2003; Jackson, 2001; continued through the 1300s, preceding the Steneck & Carlton, 2001). sequential activities of English, German, and The North Atlantic Ocean is one area in which Danish traders from the 1400s to the 1700s the coastal marine communities are often a blurred (Karlsson, 2000; Byock, 2001; Jones, 2001). mixture of species that have colonized naturally Additionally, as the need for fish in Catholic and those that have been introduced by humans. Europe developed in the mid-1300s, innumerable As Carlton (2003) has noted, it is often assumed fishing vessels began to journey between coastal that the species composition of marine commu- European countries and the fishing grounds off the nities in the North Atlantic before the advent of central islands (particularly Iceland), as well as to the eastern North American coast (particularly Correspondence to: J. A. Coyer. e-mail: [email protected] Newfoundland; Lindroth, 1957; Buckland, 1988;

ISSN 0967-0262 print/ISSN 1469-4433 online/06/020235–246 ß 2006 British Phycological Society DOI: 10.1080/09670260600652820 J. A. Coyer et al. 236

Karlsson, 2000). Consequently, numerous avenues and Shetlands (Lu¨ ning, 1990; Hardy & Guiry, and mechanisms existed for human-induced intro- 2003). It was accidentally introduced to the north- ductions of marine species throughout the North western Atlantic (Nova Scotia) in the late 1880s Atlantic well before the ‘‘benchmark’’ biological (Hay & MacKay, 1887; Robinson, 1903; Edelstein surveys of the mid-1800s. et al., 1971–73). The species also is a dominant Marine macroalgae are easily transported from member of the intertidal community along c. one area to another by shipping or fisheries. 100 km of southwestern Iceland and offshore Historically, the most common method probably Heimaey, as well as in a single fjord in the was via rock ballast. For example, the type of Faroes (Trongisva´ gsfjørôur on the southernmost Viking ship (kno¨rr) widely used for transit between island of Suôuroy; Bruntse et al., 1999; Iceland and Norway required 16 tons of ballast Gunnarsson & Jo´ nsson, 2002). Collection records stones or weighted cargo (Buckland & Sadler, indicate that it was present off Iceland and the 1990) and algal species could have survived for Faroes before 1900, although the record from the several days in the damp holds while attached to Faroes is highly doubtful (Jo´ nsson, 1903; Bruntse the ballast, assuming that the ballast was collected et al., 1999). from intertidal or shallow subtidal habitats. Given its life history characteristics, it is almost Seaweeds have also been used as fodder for sheep certain that F. serratus was introduced to Iceland and cattle in the Icelandic settlements (Amorosi and the Faroes by humans. It is dioecious, et al., 1998 and references therein) and it is perennial (3–4 years), and reproduces sexually reasonable to expect that seaweeds were used to (annually) with no vegetative reproduction, either sustain livestock during the several-day transit via holdfast sprouting or vegetative propagules from Scandinavia to Iceland/the Faroes in the (Malm et al., 2001). Dispersal of eggs is restricted open-decked knerrir. Contemporary methods of to within 1–2 m of the parent (Arrontes, 1993), introduction include the use of seaweed as packing although distances >6 m are possible, as have been material for invertebrate fisheries, microscopic life reported for F. vesiculosus and the related genus, stages accompanying oysters as they are shipped Ascophyllum (Serraõ et al., 1997; Dudgeon et al., worldwide, and entanglement of reproductive 2001; Engel et al., 2005). The genetic consequences fragments in fishing gear (reviewed in Siguan, of low dispersal were demonstrated in a recent 2003; Miller et al., 2004 and references therein). population genetic study showing that the panmic- Well-studied examples of recent (<50 years ago) tic unit for F. serratus was between 0.5 and 2 km macroalgal introductions include the large brown (Coyer et al., 2003). Dispersal is further limited algae Undaria pinnatifida and Sargassum muticum because: (i) the egg-produced pheromones effec- and the green algae Codium fragile subsp. tomen- tively attract sperm only within distances of tosoides and Caulerpa taxifolia (reviewed in Walker micrometers to millimeters (Serraõ et al., 1996); & Kendrick, 1998; Siguan, 2003; see also, Jousson (ii) nearly 100% fertilization success of gametes et al., 1998; Trowbridge & Todd, 1999a, b; is possible only when release occurs during Meusnier et al., 2002; Thornber et al., 2004; calm water conditions (Pearson & Brawley, 1996; Provan et al., 2005; Voisin et al., 2005). Two Serraõ et al., 1996; Pearson et al., 1998); and (iii) examples of older introductions (>100 years ago) fertilization success decreases rapidly with increas- are Fucus evanescens and F. serratus, both of which ing water motion (Pennington, 1985; Denny & are major components of rocky intertidal com- Shibata, 1989; Levitan et al., 1992), which munities on North Atlantic shores. The former is obviously separates the gametes and negates the a circumpolar species, occurring in the North influence of pheromones. Because thalli lack Pacific, as well as off northeastern North flotation vesicles, they sink when detached, so America, Greenland, Spitzbergen, Iceland, and that open ocean rafting between either Iceland or northwestern Norway (Powell, 1957; Lu¨ ning, the Faroes from Northern Europe is unlikely 1990). It was accidentally introduced into the because of: (i) the distance (300 km from the Oslofjorden (southeastern Norway) in the mid- British Isles to the Faroes; 400 km from the 1890s and expanded to southern Sweden by 1966 Faroes to Iceland; 900 km from Iceland to and the western Baltic by 1992 (Schueller & Peters, Norway); (ii) depths (>500 m); and (iii) the 1994; Wikstro¨ m et al., 2002). Furthermore, prevailing west-to-east flowing Gulf Stream. F. evanescens has hybridized extensively with Additionally, F. serratus has never been recorded the native F. serratus in the Blushøj region on from Greenland (Jo´ nsson, 1912; Lund, 1959; Denmark’s Kattegat coast (Coyer et al., 2002a). Pedersen, 1976), a straight-line distance of 600 km The closely related F. serratus is a northeastern from its present distribution in southwestern Atlantic species, ranging from the northern Iberian Iceland. Peninsula to the White Sea and into the Kattegat/ A recent microsatellite-based study of F. serratus Baltic Seas, as well as throughout the British Isles populations throughout its range demonstrated Origin of Fucus serratus in Iceland and the Faroes 237 a link between the single Icelandic population sampled and several populations in the Oslofjorden-Western Sweden region of the Kattegat Sea (Coyer et al., 2003). However, only one population from western Norway (Bergen) was sampled and none from the Faroes or Scotland. In the present investigation, we supplemented earlier samples by sampling seven additional sites in both Iceland and western Norway, and one each from the Faroes and the Orkneys. Microsatellite loci offer a powerful means by which to assess putative sources of introduced populations (e.g. Aguilar et al., 2005; Genton et al., 2005). Accordingly, we analysed genetic variation at several microsatellite loci to: (i) determine if there was one or multiple introductions to Iceland and the Faroes; (ii) identify a source or sources for the introduced populations; and (iii) determine if hybridization has occurred between introduced F. serratus and native F. evanescens in Iceland, which could have been sympatric for c. 1,000 years, as it has in the Kattegat Sea where the introduced F. evanescens and native F. serratus have been Fig 1. Location of samples and pathways of introduction. sympatric for only about 100 years (Schueller & (A): Karlshamn; (B): Gjerrild; (C): Sma˚skjaer; (D): Bergen; ˚ Peters, 1994; Wikstro¨ m et al., 2002). (E): Alesund; F: Trondheim; (G): Bodø; (H): Tromsø; (I): Nyborg; (J): Kirkenes; (K): Grense-Jakobselv; (L): The Faroes (Suôuroy); (O): Orkneys; (P): Ireland (Limerick). Materials and methods Iceland (insert): (1): North Seltjarnarnes; (2): South Seltjarnarnes; (3): Hafnarfjo¨ rôur; (4): Vatnsleysa; (5): Sampling Garôskagi; (6): Sandgerôi; (7): Stafnes; (8): Heimaey. For all populations, individuals were collected at about 1-m intervals along a transect line. For each individual, a 1-cm piece from 4–6 apical tips was excised and placed into silica gel crystals for rapid dehydration and storage Data analysis as described earlier (Coyer et al., 2003). Seven populations collected off Iceland supplemented the single Descriptive statistics of genetic diversity (allelic richness; population and collectively spanned the entire range of observed heterozygosity, Hobs; Nei’s gene diversity, F. serratus on Iceland: (1): North Seltjarnarnes (sampled Hexp; Nei, 1978), as well as estimators of FIS and FST earlier [Coyer et al., 2003]); (2): South Seltjarnarnes; (Wright, 1969; as f and , Weir & Cockerham, 1984) (3): Hafnarfjo¨ rôur; (4): Vatnsleysa; (5): Garôskagi; (6): were estimated (and tested with 2000 permutations) Sandger i; (7): Stafnes; and (8) Heimaey (numbers using the GENETIX 4.02 program (Belkhir et al., 2001). ô locus correspond with locations in Fig. 1). Seven populations Additionally, the mean number of alleles was of F. serratus along the western Norwegian coast normalized to a sample size of 36 (equal to the smallest supplemented earlier samples from the Oslofjorden (C) sample at Kirkenes) using the GENCLONE 1.0 ( and Bergen (D) (Coyer et al., 2003), thereby spanning version) program (Arnaud-Haond & Belkhir, available the entire range of F. serratus in Norway: A˚lesund (E), on request from [email protected]) and a re-sampling Trondheim (F), Bodø (G), Tromsø (H), Nyborg (I), of 1,000. Pairwise distances among all population pairs Kirkenes (J), and Grense-Jakobselv (K) (letters corre- were calculated from allele frequency data of seven spond to locations in Fig. 1). A single population was microsatellite loci (Coyer et al., 2003) using the program sampled from Trongisva´ gsfjørôur, Suôuroy, the Faroes GENETIX 4.02 (Belkhir et al., 2001). The 22 popula- (L) and from Ferry Pier on Rousay Island, Orkneys (O). tions included one population from each of the three internal clusters within the Skagerrat/Kattegat/Baltic cluster described earlier (Coyer et al., 2003): Sma˚skjaer DNA extraction and microsatellite analysis (C; Norway) from the Western Sweden cluster, Gjerrild DNA was extracted from c. 40 mg of silica-dried tissue (B; Denmark) from the Eastern Denmark cluster, as previously described (Coyer et al., 2002b). and Karlshamn (A; Sweden) from the Lower Baltic Subsequent PCR amplification, determination of geno- cluster, as well as Limerick, Ireland (P; Fig. 1). types with seven microsatellite primers (FsA198, The Cavalli-Sforza and Edwards’ chord distance FsB113, FsB128, FsD39, FsE6, FsE9, FsF4), and (Cavalli-Sforza & Edwards, 1967) was chosen, as this visualization of genotypes with an automated sequencer measure has been shown to generate higher probabilities are described elsewhere (Coyer et al., 2002b). of obtaining the correct tree topology (Takezaki & J. A. Coyer et al. 238

Nei, 1996). Cavalli-Sforza and Edwards’ chord distances FsB113, FsB128, FsD39, FsF4) used for a study of were computed using GENDIST. Neighbour-joining F. serratus F. evanescens hybridization in Denmark was used to construct the tree in NEIGHBOR, whereas (Coyer et al., 2002a). Tissue samples were collected from bootstrap re-sampling (1,000 replications) was per- 36 individuals of F. serratus and 34 individuals of formed using SEQBOOT and CONSENSE. All pro- F. evanescens displaying species-specific morphology grams are part of the software package PHYLIP 3.5 and from 18 individuals with an intermediate morphol- (Felsenstein, 1994). ogy (¼putative hybrids; see photos in Coyer et al., To determine the most likely European source for all 2002a) from Heimaey. Microsatellite genotypes were Icelandic populations, we used an assignment test, which analyzed with STRUCTURE (Pritchard et al., 2000), evaluates a set of reference populations as possible which uses a Bayesian algorithm to identify K user- origins of individuals or groups of individuals based on defined clusters of individuals that are genetically multilocus genotypes and expresses the evaluation as homogeneous. Sampled individuals are assigned either a log-likelihood (Piry et al., 2004). We used genotypes to clusters or jointly to two or more clusters if their from the seven microsatellite loci and the software genotypes indicate admixture. This approach has been GENECLASS2 (Piry et al., 2004) to evaluate Icelandic used recently to study hybridization in Fucus (Engel populations to reference European populations; simi- et al., 2005) and, as it is based on probability, is more larly we determined the likely source for the Faroese powerful than the graphical approaches, such as population. The assignments were based on Rannala Factorial Correspondence Analysis, that have been and Mountain’s (1997) Bayesian method, as well as the used previously (Coyer et al., 2002a; Wallace et al., allele frequency based method of Paetkau et al. (1995), 2004). All analyses were replicated 10 times to ensure and chord distance (Cavalli-Sforza & Edwards, 1967). proper convergence of the MCMC with the parameters: Assignment scores reflect the relative strength of the log- ancestry model ¼ admixture (to account for recent likelihood value associated with a given reference divergence and shared ancestral polymorphisms); population. A score of 100% reflects that the likelihood frequency model ¼ independent; burn-in ¼ 1,000,000; of a population being the source is 100%. Any value MCMC length ¼ 2,000,000 after burn-in, and K ¼ 2. less than 100% reflects the possibility that alternative populations are the source, but no confidence limits are calculated for assignment scores. Because we are Results interested in a historical introduction, as opposed to The Iceland/Faroes cluster was highly resolved detection of first-generation migrants, we used a group (rather than individual) assignment, thereby (bootstrap ¼ 90%) from the other populations integrating the various multilocus genotypes and (Fig. 2). Within Iceland, the two populations reducing the bias associated with an unknown time of furthest from Hafnarfjo¨ rôur, namely Sandgerôi introduction. and Stafnes, were strongly supported (boot- Molecular verification of hybridization was through strap ¼ 82%) from the other Icelandic populations. the analysis of the same five microsatellite loci (FsA198, Yet, the most isolated Icelandic population of

Fig 2. Neighbour-joining tree illustrating the relationships among populations of Fucus serratus in Northern Europe. The tree was based on chord distance (Cavalli-Sforza & Edwards, 1967); bootstrap values were derived from 1,000 permutations of allele frequencies. Letters and numbers as in Fig. 1. Origin of Fucus serratus in Iceland and the Faroes 239

Table 1. Log-likelihood values from an assignment test for Icelandic populations of Fucus serratus using the Rannala and Mountain (1997) method. The assignment scores for Sma˚skjaer are 100%. All potential source locations in the left column are in Norway except Gjerrild (Denmark), Karlshamn (Sweden), Orkneys (Scotland), and Limerick (Ireland). Letters and numbers correspond with locations in Fig. 1.

North South Seltjarnarnes Seltjarnarnes Hafnarfjo¨ rôur Vatnsleysa Garôskagi Sandgerôi Stafnes Heimaey (1) (2) (3) (4) (5) (6) (7) (8)

Smaskjær (C) 119.224 130.239 127.749 132.588 123.116 112.486 105.796 135.141 A˚lesund (E) 157.179 163.124 163.606 167.810 169.369 152.534 150.129 154.825 Bodø (G) 169.458 173.497 175.114 170.343 184.041 164.477 157.849 180.956 Gjerrild (B) 174.293 190.590 187.815 196.818 183.494 162.046 154.568 207.320 Tromsø (H) 182.294 173.393 173.987 189.382 191.34 186.139 186.090 156.964 Trondheim (F) 182.991 188.486 184.943 209.614 194.469 176.126 177.646 200.712 Kirkenes (J) 205.336 202.897 212.109 216.534 209.492 192.892 187.665 177.860 Grense-Jakobselv (K) 209.020 206.022 218.496 223.179 217.331 220.208 223.777 200.258 Nyborg (I) 216.668 214.632 220.726 239.076 240.084 247.528 245.281 234.899 Karlshamn (A) 228.138 246.499 239.754 233.205 255.098 240.383 221.161 220.672 Orkneys (O) 247.246 248.723 253.781 268.319 266.591 252.561 244.627 237.713 Limerick (P) 308.814 324.462 321.552 332.684 347.596 327.620 322.275 333.300 Bergen (D) 351.217 352.953 369.867 389.509 375.576 349.251 349.555 395.302

Fucus serratus, on offshore Heimaey, was not Table 2. Assignment of the populations of Fucus serratus separated despite possessing the longest branch on the Faroes to Icelandic populations. Letters and length (Fig. 2). Furthermore, branch lengths of the numbers correspond with locations in Fig. 1.

Iceland/Faroes cluster were short relative to other Faroes (L) branch lengths between non-Icelandic populations, suggesting a higher degree of overall relatedness Potential source location Log-likelihood Assignment scores among the Icelandic populations. A cluster of Hafnarfjo¨ rôur (3) 29.830 83.254 Orkneys/Bergen/Ireland was moderately supported South Seltjarnarnes (2) 30.528 16.693 (bootstrap ¼ 73%) and the Bergen/Ireland popula- North Seltjarnarnes (1) 33.303 0.028 tions were highly resolved within this cluster Garôskagi (5) 33.364 0.024 Vatnsleysa (4) 34.850 0.001 (bootstrap ¼ 88%). Stafnes (7) 42.832 0 An assignment test showed that Sma˚skjaer, a Heimaey (8) 49.390 0 small island in the Oslofjorden, was the most likely Sandgerôi (6) 49.888 0 source for all Icelandic populations (Fig. 1; Sma˚skjaer (C) 138.945 0 A˚lesund (E) 155.300 0 Table 1). This result was also obtained using an Bodø (G) 162.975 0 allelic frequency method (Paetkau et al., 1995) and Tromsø (H) 177.333 0 a distance-based method (Cavalli-Sforza & Gjerrild (B) 186.613 0 Edwards, 1967; data not shown). The single Trondheim (F) 192.353 0 Kirkenes (J) 206.742 0 Faroese population at Trongisva´ gsfjørôur Grense-Jakobselv (K) 224.666 0 (Suôuroy) was assigned to Hafnarfjo¨ rôur Nyborg (I) 231.288 0 (Iceland), a major harbour area on the south- Karlshamn (A) 234.890 0 Orkneys (O) 258.280 0 western coast (Table 2). Ireland (P) 332.364 0 Although not significant, genetic diversity in Bergen (D) 388.890 0 Sma˚skjaer (Hexp ¼ 0.587) appeared higher than in all mainland Icelandic samples (Hexp ¼ 0.411– 0.441), consistent with a source–sink relationship (Table 3). Similarly, genetic diversities in Heimaey populations, 0.299 (0.004) for Heimaey, and 2.80 (Hexp ¼ 0.317) and the Faroes (Hexp ¼ 0.367) (0.002) for the Faroes (Table 3). appeared lower than in Icelandic sources, Pairwise FST estimates revealed significant popu- compatible with an introduction from mainland lation structure among European populations Iceland. The same trend was apparent for allelic (0.0910–0.6939) and among European and diversity as well, with the mean number of Icelandic/Faroese populations (0.1358–0.6246; alleleslocus (normalized for a sample size of 36) Appendix I). Estimates among populations off and a re-sampling-based standard error was 7.17 Iceland and the Faroes showed both significant (0.012) for Sma˚skjaer, 0.281 (0.002) to 0.391 (0.0338–0.1765) and non-significant (0.0041, (0.006) for the seven ‘‘mainland’’ Icelandic 0.0090) structure. J. A. Coyer et al. 240

Table 3. Genetic diversity of Fucus serratus. Letters and numbers in the first column correspond with locations in Fig. 1.

ˆ Location NA A SE Hexp Hobs FIS

Karlshamn (A) 50 5.57 5.10 0.007 0.458 0.434 0.052 Gjerrild (B) 56 8.57 7.18 0.011 0.517 0.525 0.016 Sma˚skjaer (C) 74 8.57 7.17 0.012 0.587 0.575 0.019 Bergen (D) 92 8.85 6.87 0.012 0.571 0.492 0.138* A˚lesund (E) 50 7.00 6.49 0.008 0.616 0.574 0.068* Trondheim (F) 49 7.43 6.75 0.009 0.636 0.557 0.126*** Bodø (G) 50 4.14 3.70 0.008 0.331 0.363 0.097* Tromsø (H) 41 6.14 5.88 0.006 0.513 0.449 0.125*** Nyborg (I) 50 4.29 3.88 0.008 0.342 0.328 0.040 Kirkenes (J) 36 2.41 2.41 0 0.182 0.135 0.262*** Grense-Jakobselv (K) 39 2.71 2.54 0.002 0.165 0.151 0.085 Ice 1 45 4.14 3.91 0.006 0.439 0.444 0.011 Ice 2 49 2.86 2.81 0.002 0.441 0.469 0.064 Ice 3 46 3.71 3.54 0.004 0.415 0.376 0.095* Ice 4 56 3.14 2.96 0.004 0.419 0.443 0.061 Ice 5 55 3.43 3.23 0.005 0.421 0.449 0.068 Ice 6 50 3.14 3.07 0.020 0.412 0.454 0.102* Ice 7 47 3.00 2.94 0.003 0.411 0.435 0.057 Ice 8 50 3.14 2.99 0.004 0.317 0.334 0.055 The Faroes (L) 51 2.86 2.80 0.002 0.367 0.336 0.086* Orkneys (O) 48 11.14 10.29 0.012 0.724 0.631 0.129*** Ireland (P) 49 7.57 7.19 0.006 0.675 0.618 0.086**

A: mean number of alleleslocus; Aˆ: mean number of alleleslocus normalized to a sample size of 36 (see text); SE: re-sampling-based (n ¼ 1,000) standard error; Hexp: Nei’s gene diversity; Hobs: observed heterozygosity. Significance values for FIS are: *<0.05, **<0.01, ***<0.001 using 2,000 permutations (see text).

1.0 Fig 3. Microsatellite characterization and detection of hybrids by the program STRUCTURE (Pritchard et al., 2000). Each individual is represented in the figure by a vertical bar partitioned into black or grey segments. The length of each segment is proportional to the individual’s membership in 0.5 each of two clusters (K) repre- senting the parental species, thereby providing a quantita- tive illustration of introgression. Grey represents F. serratus (n ¼ 36) and black corresponds to F. evanescens (n ¼ 34). Individuals between the two baseline ticks (n ¼ 18) are morphologically intermediate individuals. K ¼ 2, ln 0.0 likelihood ¼422.8. F. serratusHybrids F. evanescens

Analysis of individuals with a morphology Discussion intermediate between F. serratus and F. evanescens Iceland revealed that eight of 18 were F1 hybrids with 50% of the alleles stemming from each parent (Fig. 3). Icelandic populations of Fucus serratus stemmed Variable levels of introgression were apparent in from a single introduction and were most closely the remaining 10 individuals. linked with a population from Sma˚skjaer, a small Origin of Fucus serratus in Iceland and the Faroes 241 island in the central portion of the Oslofjorden in Trade between Iceland and Scandinavia southeastern Norway (Fig. 1, Table 1). The eight (primarily Norway) was minimal during the Icelandic populations were clearly not derived Settlement/Viking/Commonwealth Eras (890– from any refugial populations that may have 1262) and the period immediately following the existed in Iceland during the last ice age Norwegian dependency (1262–1380) because (18,000–20,000 years BP), although genetic evi- of limited agricultural production and a lack of dence for terrestrial plants (reviewed in Caseldine commercial fisheries (Karlsson, 2000; Byock, et al., 2004) and marine invertebrates and verte- 2001). Early trade was difficult and time-consum- brates (Holder et al., 1999; Wares, 2001, 2002; ing, as the merchants arrived in summer and Wares & Cunningham, 2001; Govindarajan et al., invariably remained until the following year 2005) suggest that glacial refugia were present in because trading could not be completed before Iceland during this time. As the introduction the arrival of winter and perilous sailing conditions undoubtedly was due to humans, the timing must (Byock, 2001). No durable warehouses or other be between c. 874, with the arrival of the first buildings involved in trade were built until the late intentional settlers, and 1900 when F. serratus was 1700s (Reynarsson, 1999; Karlsson, 2000). noted in the first comprehensive marine survey Trade became more important from the mid- of Iceland (Jo´ nsson, 1903). The distribution of 1300s, as Icelandic stockfish (dried cod) helped F. serratus in 1900 was much more restricted feed the high demand for fish in Europe. The than now, being confined then to Hafnarfjo¨ rôur considerable stockfish trade was initiated by (‘‘3’’ on Fig. 1) where it ‘‘grew gregariously’’, Norwegian merchants who conveyed the fish to and Heimaey (‘‘8’’ on Fig. 1), an island 10 km Bergen, which was controlled by the German offshore (but about 130 km from the nearest Hanseatic League (Karlsson, 2000). Despite the extant population of F. serratus on the mainland early trade with Bergen, the population of F. serratus in Bergen was not linked to the Icelandic and 180 km from Hafnarfjo¨ rôur), where populations in our assignment test. it ‘‘occurred rarely’’ (Jo´ nsson, 1903). The During the subsequent ‘‘English Century’’ (early present distribution along about 100 km of 1400s to mid-1500s) of Icelandic history, English southwestern coast (excluding Heimaey) represents fishing vessels (about 10 large vessels each year) an average expansion from Hafnarfjo¨ rôur since plied the waters off southern Iceland and the 1900 of c. 0.3 and 0.6 km yr1 to the north and fishermen established a main fishing camp on south, respectively, and is consistent with the size Heimaey and a secondary camp at Grindavik on of the F. serratus panmictic unit (0.5–2.0 km) the southern Iceland coast (Karlsson, 2000). The (Coyer et al., 2003). rare occurrence and absence, respectively, of F. Iceland’s first intentional settlers arrived in 874 serratus from these areas in 1900 (Jo´ nsson, 1903), from a region in Norway between Bergen and ˚ together with the rejection of Ireland and the Alesund and spent the first winter at Ingo´ lfsho¨ fôi Orkneys as sources by the assignment tests, imply on the southern coast where F. serratus has never that English fishing/trading activities were not been reported (Jo´ nsson, 1903; Gunnarsson & responsible for the introduction of F. serratus to Jo´ nsson, 2002). They settled permanently in the Iceland. Furthermore, during the German period Reykjavı´ k area (8 km north of Hafnarfjo¨ rôur) of influence in the latter half of the 1500s, fishing during the following summer and claimed much activities and trade were almost exclusively with of southwestern Iceland, including the area encom- Hamburg (Karlsson, 2000), a port 100 km inland passing the current distribution of F. serratus on the River Elbe and an improbable source for (except for Heimaey; Book of Settlements, the marine F. serratus. Pa´ lsson & Edwards, 1972). Immigration accounts Iceland fell under Danish control from the mid- reveal that, during the Age of Settlement (890– 1500s to the mid-1800s and, during this time, the 930), 10,000–20,000 people emigrated to Iceland, population fluctuated between 30,000 and 60,000 most from Norway (Reynarsson, 1999; Byock, (down from about 76,000 in 1100) because of 2001). Most of the Norwegian settlers to Iceland’s the plague, the Danish-imposed trade monopoly, South Quarter, where F. serratus is confined today and famines associated with a colder climate and and which included the first settler’s claim as well volcanic eruptions (Reynarsson, 1999; Karlsson, as areas further east, came from the Bergen to 2000; Byock, 2001). The Danish trade monopoly Bodø (north of A˚lesund) region of western from the early 1600s to the late 1700s favoured Norway (Pa´ lsson & Edwards, 1972). Four of our traders from the Copenhagen-lower Baltic area sampled populations were within the Bergen (Karlsson, 2000); again, areas that were not linked to Bodø region and four more from areas further to the Icelandic populations by our assignment north, but none were significantly linked to tests. After trade sanctions were lifted, other Iceland (Table 1). countries gradually initiated trade with Iceland. J. A. Coyer et al. 242

Fishing and whaling stations were built around especially the southwestern coast where F. serratus the coast, Reykjavik began to grow from the currently is restricted, and noted the presence mid-1700s (exponentially by the early 1800s), and of numerous algal species that today co-occur imported timber became the dominant building with F. serratus. It is difficult to believe that he material in Icelandic towns (Reynarsson, 1999; could have missed a large species like F. serratus, Karlsson, 2000). a dominant member of the intertidal community Timber has been a major export of Norway for and easily distinguished from all other species centuries. During the Viking Era, relatively small of Fucus. quantities of timber were shipped to Iceland for Secondly, F. serratus may have existed as a structures and ship building as the Icelandic birch/ highly localized population in the Hafnarfjo¨ rôur willow forests and supply of drift timber were area for centuries before expanding its range inadequate for these purposes (Mageroey, 1993; shortly after the 1900 survey. Few introduced Byock, 2001). Norway completely dominated populations are completely unconstrained in their the world timber market from around 1520 to growth, as mortality influences all life stages and 1880 when huge volumes were logged from the low numbers of invading dioecious individuals Oslofjorden (area of Sma˚skjaer) to meet the (such as F. serratus) decrease the probability of increasing demand from Europe (Rolstad et al., successful fertilization and subsequent coloniza- 2002). In addition to commercial logging, many tion/expansion. Consequently, it is not uncommon farms in the Oslofjorden also were involved in for introduced species to remain at very low the export of timber (Eier, 1969, see also population levels for years and/or require decades www.frogn.historielag.org). for exponential population growth. For example, The immediate area of Sma˚skjaer also was the Pacific oyster was introduced on a nearly strategically important as a winter harbour annual basis to the Netherlands from 1964 to 1971; during this time because the main harbours of reproduction was noted in the Oostershelde Drammen and Oslo in the innermost regions of the estuary beginning in 1975, with explosive growth Oslofjorden were frozen during winter months. in the estuary in the mid-1980s and expansion Consequently, cargo exchange occurred in the along the entire Dutch coast by 2000 (Wolff & nearby and ice-free port of Drøbak (1 km from Reise, 2002). Thus, it is at least possible that F. Sma˚skjaer) and, when the harbour was congested, serratus could remain in a localized population for many ships moored to iron rings fastened on small hundreds of years before expanding its distribu- islands (such as Sma˚skjaer) before gaining access tion, although it seems highly unlikely. to Drøbak (Eier, 1969). From a transport and Alternatively, it is possible that F. serratus was introduction standpoint, it is significant that ships introduced much later, perhaps during the mid- were most likely to be moored to the islands during 1700s to the late-1800s. It must be remembered winter and early spring when F. serratus is that for 1,000 years, from the late-800s to the early- reproductive (Fredriksen, 1990). 1800s, all of Iceland was essentially a farmstead In summary, the coupling of trade history and with no towns or villages and a population our assignment tests suggests that the introduction fluctuating between 30,000 and 60,000 until of F. serratus to Iceland from the Sma˚skjaer exponential growth began in the early-1800s area of Norway most likely occurred during (Karlsson, 2000). As human-induced species intro- either 900 to the late-1300s (Settlement/Viking/ ductions are likely to be positively correlated with Commonwealth/Norwegian Kingdom Eras) or levels and rates of human colonization, the chances from the mid-1700s to the late-1800s, when of introduction should be higher during rapid exported timber supplied the needs of a rapidly population growth and expansion (c. 900–1100 and growing urban Iceland. But which period is more mid-1800s) and lower during steady-state or likely? In the absence of a molecular clock, due to decline (c. 1200–1800). the lack of a fossil record or dated vicarance event, The history of the Oslofjorden, particularly dur- the answer must be speculative. ing the Settlement/Viking/Norwegian Kingdom If F. serratus was introduced during the Eras (900 to late 1300s) and the mid-1700s to first period, why didn’t it expand beyond late-1800s, is consistent with the area being a Hafnarfjo¨ rôur, the only mainland location where realistic source of F. serratus for Iceland. The it was present in 1900? Two possibilities exist. later, rather than earlier, time of introduction First, F. serratus may have been more widespread is suggested, because of: (i) the highly limited in distribution than acknowledged during the 1900 Icelandic distribution of F. serratus in 1900, survey (Jo´ nsson, 1903). This is unlikely, however, and (ii) the minimal genetic resolution of as Jo´ nsson surveyed intertidal and subtidal habi- F. serratus populations within Iceland (Fig. 2; tats around the entire perimeter of Iceland, Appendix I). Origin of Fucus serratus in Iceland and the Faroes 243

The Faroes hybridization – whether it is prevented by pre- or post-zygotic mechanisms, leads to widespread Despite the importance of the Faroes to both the introgression (as revealed among a randomly discovery and settlement of Iceland (Jones, 2001), selected group of individuals), or results in a new the single Faroese population of F. serratus is most species – remains to be determined. likely to have originated from the Icelandic Genetic data provide a powerful means harbour area of Hafnarfjo¨ rôur, as revealed by the by which to track spatial pathways or identify assignment tests and the non-significant pairwise source–sink components of species introductions. F estimate. The species was noted in the Faroes ST Establishing temporal aspects of introduction (Trongisva´ gsfjørôur) in 1997 and was viewed as pathways, however, can be problematic if the a recent introduction because it was not present genetic marker used is invariant over the number anywhere off the Faroes during marine surveys of generations that have elapsed since the putative conducted in 1819, 1870, 1902, and 1982 (Bruntse introduction. Combining genetic data with careful et al., 1999 and references therein). Consequently, scrutiny of historical records of trade and other both historical survey data and genetic data commerce between the source and sink, however, (assignment tests, genetic diversity, population can help to provide reasonable temporal estimates. structure) of the single known population suggest strongly that F. serratus was introduced to the Faroes sometime between 1982 and 1997 by an Acknowledgments unknown mechanism. At present, a few fishing vessels and the daily ferry to the capital at We are grateful to J.A. Berges, J.L. Berges, E. Boon, To´ rshavn utilize the natural harbour of S. Ferber, J.B. Heiser, and A. Peters for assistance Trongisva´ gsfjørôur. with sample collections. We also thank A. Ingo´ lfsson, The late 20th century introduction from Iceland K. Gunnarsson, and P. Buckland for insightful to the Faroes also indirectly supports a later comments; A. Andreasen, B. Geyti, and K. Gunnarsson for logistical support in the Faroes; (rather than earlier) introduction of F. serratus to K. Gunnarsson, G. V. Helgason, R. Sweinsson, and Iceland from Sma˚skjaer. The Faroes were a very H. Halldo´ rsson for logistical support in Iceland; important region during the Viking/Norwegian T. Koevoets for help with figures, and D. Haydar and Kingdom Eras and ships from Norway frequently an anonymous reviewer for comments on an earlier stopped at the Faroes before going on to Iceland. version of the manuscript. This study was supported If F. serratus was introduced to Iceland during the in part by the BIOBASE Project funded under early periods, a Norway to Faroes to Iceland path EU MAST III, Control Number PL97-1267; the should be revealed by the genetic diversity, not the IHP (Improving Human Potential) Programme of decreasing gradient in genetic diversity (Hexp, the European Commission (for work at the Sandgerôi allelic richness) we observed from Sma˚skjaer to Marine Center in Iceland); and the Netherlands Iceland to the Faroes. Organization for the Advancement of Research (Grant Number 813.04.008).

Hybridization Two lineages are present within the genus Fucus: References (i) F. serratus and F. distichus (evanescens), and (ii) AGUILAR, A., BANKS, J.D., LEVINE, K.F. & WAYNE, R.K. (2005). F. vesiculosus and F. spiralis (Serra˜o et al., 1999; Population genetics of northern pike (Esox lucius) introduced Coyer et al., 2006). Hybridization readily occurs into Lake Davis, California. Can. J. Fish. Aquat. Sci., 62: 1589–1599. among members of a lineage, but is not common AMOROSI, T., BUCKLAND, P.C., EDWARDS, K.J., MAINLAND, I., between lineages (Coyer et al., 2002a; Wallace MCGOVERN, T.H., SADLER,J.&SKIDMORE, P. (1998). They et al., 2004; Engel et al., 2005; Billard et al., 2005, did not live by grass alone: the politics and palaeoecology of Coyer, unpubl. data). The presence on Iceland of animal fodder in the North Atlantic region. Envir. Archaeol., 1: 41–54. F1 hybrids between the introduced F. serratus and ARRONTES, J. (1993). The nature of the distributional boundary of the native F. evanescens, as well as in Denmark Fucus serratus on the north shore of Spain. Mar. Ecol. Prog. Ser., between the introduced F. evanescens and the 93: 183–193. native F. serratus (Coyer et al., 2002a), indicates BELKHIR, K., BORSA, P., GOUDET, J., CHIKHI,L.&BONHOMME,F. (2001). GENETIX, logiciel sous WindowsTM pour la genetique that hybrids and hybrid zones can be expected in des populations, Laboratoire Genome et Populations. Universite´ early stages of sympatry, regardless of which de Montpellier II, France. species arrived first. Furthermore, introgression BILLARD, E., SERRA˜O, E., PEARSON, G.A., ENGEL, C.R., was apparent among individuals deliberately DESTOMBE,C.&VALERO, M. (2005). Analysis of sexual penotype and prezygotic fertility in natural populations of F. spiralis, chosen because they were morphological inter- F. vesiculosus (Fucaceae, Phaeophyceae) and their putative mediates to the parents. The outcome of hybrids. Eur. J. Phycol., 40: 397–407. J. A. Coyer et al. 244

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Appendix I. Population differentiation of Fucus serratus. Above diagonal: pairwise estimates of (Weir & Cockerham, 1984) tested by 2,000 permutations; Below diagonal: corresponding p- values (***p 0.001). Sampling sites (letters and numbers correspond to locations in Fig. 1: Ksh (A), Karlshamn; Gje (B), Gjerrild; Sma (C), Sma˚skjaer; Ber (D), Bergen; Ale (E), A˚lesund; Trd (F), Trondheim; Bod (G), Bodø; Trm (H), Tromsø; Nyb (I), Nyborg; Kir (J), Kirkenes; GJ (K), Grense-Jakobselv; Ice 1, North Seltjarnarnes; Ice 2, South Seltjarnarnes; Ice 3, Hafnarfjo¨ rôur; Ice 4, Vatnsleysa; Ice 5, Garôskagi; Ice 6, Sandgerôi; Ice 7, Stafnes; Ice 8, Heimaey (Vestmannaeyjar); Far (L), Suôuroy, The Faroes; Ork(O), Rousay Island, Orkneys; and Ire (P), Limerick.

Ksh Gje Sma Ber Ale Trd Bod Trm Nyb Kir GJ Ice 1 Ice 2 Ice 3 Ice 4 Ice 5 Ice 6 Ice 7 Ice 8 Far Ork Ire

Ksh (A) – 0.3057 0.2581 0.3666 0.3155 0.3721 0.4433 0.3650 0.5595 0.5599 0.5914 0.3992 0.4116 0.4274 0.3889 0.4194 0.4138 0.4051 0.4236 0.4387 0.2863 0.3492 Gje (B) – 0.0910 0.2779 0.2200 0.2058 0.3986 0.3438 0.4009 0.3913 0.4727 0.2829 0.3230 0.3356 0.3186 0.2893 0.2726 0.2690 0.4035 0.3595 0.2247 0.3468 Sma (C) – 0.2992 0.0967 0.1853 0.2574 0.2545 0.3842 0.3466 0.4670 0.1608 0.2054 0.1951 0.1851 0.1732 0.1527 0.1358 0.2532 0.2072 0.1657 0.3087 Ber (D) – 0.3143 0.2765 0.4274 0.3792 0.4118 0.4978 0.4171 0.3597 0.3583 0.3933 0.3732 0.3646 0.3769 0.3863 0.4483 0.4211 0.2796 0.2817 Ale (E) – 0.1576 0.2566 0.2216 0.3669 0.3548 0.4697 0.1972 0.2227 0.2119 0.2091 0.2102 0.1911 0.1792 0.2627 0.2250 0.1147 0.2913 Trd (F) – 0.3846 0.1686 0.1933 0.3538 0.3550 0.2591 0.2702 0.2817 0.2970 0.2805 0.2835 0.2848 0.3708 0.3158 0.1883 0.2780 Bod (G) – 0.4096 0.5536 0.6025 0.6939 0.2997 0.3435 0.3321 0.2840 0.3182 0.3106 0.2940 0.3934 0.3379 0.3601 0.4213 Trm (H) – 0.3127 0.4155 0.3777 0.3051 0.3247 0.3251 0.2954 0.3155 0.3409 0.3356 0.3201 0.3430 0.2141 0.3405 Nyb (I) – 0.5448 0.4609 0.4060 0.4293 0.4502 0.4360 0.4397 0.4928 0.4935 0.5213 0.4805 0.3649 0.4294 Kir (J) – 0.6430 0.5164 0.5403 0.5520 0.5236 0.5043 0.4994 0.4893 0.5604 0.5717 0.3514 0.5199 GJ (K) – 0.5590 0.5633 0.5979 0.5590 0.5502 0.5919 0.6028 0.6244 0.6246 0.4154 0.5204 Ice 1 – 0.0455 0.0264 0.0161 0.0374 0.1069 0.0765 0.1745 0.0362 0.2945 0.3637 Ice 2 – 0.0090 0.0556 0.0403 0.1054 0.1129 0.1496 0.0276 0.3056 0.3652 Ice 3 0.07 – 0.0409 0.0323 0.0935 0.0852 0.1483 0.0041 0.3127 0.3840 Ice 4 – 0.0338 0.1002 0.0832 0.1146 0.0364 0.3051 0.3762 Ice 5 0.05 – 0.0348 0.0389 0.1267 0.0460 0.2975 0.3914 Ice 6 – 0.0156 0.1566 0.0987 0.2921 0.3993 Ice 7 0.007 – 0.1765 0.0966 0.2850 0.3985 Ice 8 – 0.1143 0.3263 0.4369 Far (L) 0.002 0.17 – 0.3347 0.4082 Ork (O) – 0.2501 Ire (P) – 246