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Hybridization of the Marine Seaweeds, Fucus Serratus And Received 19March 2002 Accepted 15 May 2002 Publishedonline 6August 2002 Hybridizationof the marineseaweeds, Fucus serratus and Fucus evanescens (Heterokontophyta: Phaeophyceae)in a 100-year-oldzone of secondarycontact J. A. Coyer1* ,A.F.Peters 2, G. Hoarau1, W. T. Stam1 and J.L.Olsen 1 1Departmentof Marine Biology, Centre of Ecology and EvolutionaryStudies, University ofGroningen, PO Box14, 9750AA Haren, The Netherlands 2Marine O¨ kologie,Institut fu¨rMeereskunde, Du¨sternbrookerWeg 20, D-24105 Kiel, Germany Historically, theintertidal seaweeds Fucus serratus (Fs) and Fucus evanescens (Fe)weresympatric only along thewestern coast of Norway. In themid-1890s, Fe (monoecious)was accidentally introducedinto theOslofjord. Putative hybridization with theendemic Fs (dioecious)was observed in Oslofjordby 1977 andin theKattegat andwestern Baltic Seasby 1998. AtBlushø j, Denmark (Kattegat Sea)putative Fs ´ Fe hybrids werepresent only whendensities of Fe and Fs exceeded14 and2 m 22 ,respectively. All ofthe 58 putative hybrids that werecollected in 1999 weredioecious and intermediate in morphology. Essentially all (57 outof 58) werereproductively mature, butthe oogonia possessedfewer and more variably sizedeggs than either parent.Examination ofeach parental speciesand putative hybrids with nuclear,mitochondrial andchloroplast molecular markers conrmed theoccurrence of hybridization. Furthermore, all ofthe hybrids possessed Fe-typechloroplasts andmitochondria, indicating that only the Fe egg ´ Fs sperm pair- ing wassuccessful in the eld.The reciprocal crossof Fs egg ´ Fe sperm wasabsent in the eldand signicantly lesssuccessful in laboratory crossings.Asymmetrical hybridization has also beenreported for several speciesof plants andanimals. Keywords: Fucus;hybridization; introducedspecies; seaweed 1. INTRODUCTION placed many native halophytes asit rapidly expandedits range (Ranwell 1964; Scholten& Rozema 1990). Expandedlevels ofmarine shipping and shing have Intra- andinter-generic hybridization have beendocu- resultedin theintroduction of non-native species to mentedfor many speciesof redand brown algae, butvir- coastal habitats (Carlton 1996). With respectto marine tually all studieshave beenbased on laboratory cultures macroalgae, mostintroductions result in thedisplacement (Rueness1978; Lewis1996 a).Hybridization has been ofexisting species,which in turn,often alter local com- veried with cytological or molecular markers for only two munity dynamicsand trophic interactions.Several intro- hybrids: chromosomecounts for eld-collected ductionsof macroalgae andtheir negative consequences Pelagophycus ´ Macrocystis (Laminarales) hybrids (Lewis& have beenwell studied: Undaria pinnatida (Hay 1990; Neushul1995) andPCR detection of species-speci c Floc’h et al. 1995); Sargassummuticum (Ambrose& Nel- ITS1 nrDNA fragments for laboratory produced son1982; Viejo 1997); Codium fragile subsp. tomentosoides Alaria ´ Lessoniopsis (Laminarales) hybrids (Liptack & (Carlton &Scanlon1985); and Caulerpataxifolia Druehl 2000). Unsurprisingly, thereare nostudies of (Acade´mie desScience-Paris 1997). hybrid zonesin marine macroalgae. The potential ofthe exotic speciesto hybridize with Several speciesof Fucus (Fucales)dominate the inter- endemicspecies is an often-overlookedaspect of species tidal andshallow subtidal biomass along northernEuro- introductions.In somecases, hybridization leadsto speci- peanshorelines (Lu ¨ning 1990), wherethey exhibit a ation andthe new species signi cantly impacts local com- considerabledegree of morphological variation both munities.For example, theestuarine cord grass Spartina within andbetween populations. Putative Fucus hybrids alterniora wasaccidentally introducedto the British Isles have beenreported from the eldfor Fucus from easternNorth America in theearly 1800s, andin the vesiculosus ´ Fucus spiralis , Fucus vesiculosus ´ Fucus serratus newhabitat, producedrare andsterile hybrids with the and Fucus ceranoides ´ Fucus spiralis (Sauvageau 1909; local species, Spartinamaritima (Marchant 1967, 1968). Gard1910; Stomps1911; Burrows& Lodge1953; Asa resultof chromosomal doubling in thesterile hybrid, Scott& Hardy 1994). anewspecies emerged ( Spartinaanglica ) (Gray et al. 1991; Fucus serratus (henceforth Fs)ranges from northernPor- Raybould et al. 1991), which subsequentlyinduced major tugal tothe White Sea,Iceland, Nova Scotia,and into geomorphological changesin thetidal habitats anddis- theKattegat andsouthern Baltic Seas(Lu ¨ning 1990). The cold-waterspecies F. evanescens (henceforth Fe) occurs off NewEngland (USA), Greenland, Iceland and northwest- ernNorway (Powell 1957; Rice& Chapman 1985; Lu¨n- *Authorfor correspondence ([email protected]). ing &tom Dieck 1990). Thus, Fs and Fe are sympatric Proc.R. Soc.Lond. B (2002) 269, 1829–1834 1829 Ó 2002 TheRoyal Society DOI10.1098/ rspb.2002.2093 1830J. A.Coyer andothers Hybridizationin Fucus along portionsof Iceland and the northwestern Norweg- ian coast. Fe wasaccidentally introducedinto theOslofjord (easternNorway) in themid-1890s andthen expanded south,appearing in theSkagerrak Seain 1924, thecentral Kattegat Sea(west coast of Sweden) in 1933, andin the Kiel Bight (westernBaltic) by 1992 (seeSchueller &Pet- ers1994). Putative Fs and Fe hybrids reaching fertility in the eldinitially werereported in Oslofjordin 1977 (Lein 1984; Rice& Chapman 1985) andmore recentlyat sev- eral locationsin theKattegat towesternBaltic Seasfrom 1998 to2000 (J.A.Coyerand A. F.Peters,unpublished data).Therefore, any hybridization betweenthe native Fs andintroduced Fe in theareas occurredwithin thelast 100 years. In thepresent study we usemolecular markers toverify theoccurrence of natural hybridization between Fs and Fe. Using eld-collectedspecimens, we examined DNA polymorphism in Fs, Fe andputative Fs ´ Fe hybrids with ve microsatellite loci (nuclear),as well asITS1 (nuclear), rubisco(chloroplast) and nad11 dehydrogenase (mitochondria) genes.We believe that ourstudy is the rst toapply microsatellite genotyping andsingle-strand con- formation polymorphism (SSCP)towards veri cation of hybridization in eldpopulations ofmarine macroalgae. 2. MATERIALAND METHODS The dioecious Fs ischaracterizedby broad thalliwith serrated margins and adistinctmidrib, whereas the hermaphroditic Fe (allconceptacles on asingleindividual contain both antheridia and oogonia)have muchnarrower thalliwith no serrationsand an indistinctmidrib ( gure1). The chromosomenumber for eachspecies is 32(or34) (Lewis 1996 b).Both speciesare peren- nial.In the KielBight, Fe isreproductiveduring late winter and spring, whereas Fs isreproductiveall year long (Schueller& Pet- ers1994). Eggs and spermof the closelyrelated F.vesiculosus typicallydisperse only 0.5 and 2m,respectively, from the par- ents (Lifvergren1996). Long-distance transport may occur, however, as detachedindividuals may driftto other areas. Putative Fs ´ Fe hybrids wereobserved in April 1998, 1999 and 2000at Blush øj,near Elsega Ê rde,Denmark (56 °109 N, 10°439 E).In April 2000, the spatial distributionsof Fs, Fe and putative Fs ´ Fe hybrids weredetermined with 0.5m 2 quadrats Figure 1. Photographs of ( a) Fs, (b) Fe and (c) a Fs ´ Fe sequentiallyplaced along threetransects (19,24, 26 minlength; hybrid collected from Blushoj, Denmarkin April 1999. The 0.5m inwidth) traversing the entire Fucus beltfrom 0 to ca. size of thepencil in eachphotograph is 14.5 cm. 22mindepth. Allpost-recruit Fucus individuals(more than 10cmin length) within the quadrats werecollected, counted ted.The egg diameterswere measured with alight microscope and weighed.Very few recruitswere present. Tissue samples for at ´ 100 magni cationafter theirrelease from the oogonia. DNA extraction werecollected from 72 Fs, 70 Fe and 58 puta- The spermbehaviour was observedat low magni cation dur- tivehybrids and processedas describedin Coyer et al. (2002a). ing the crossingexperiments. The formationof spermclouds Laboratory crossesfor allcombinations of maleand female concentratedaround the eggs was interpretedas evidencefor Fs, Fe and Fs ´ Fe hybrids wereconducted as describedin Coyer chemotaxis,that has beenwell studied in Fucus spp. (Mu¨ller & et al. (2002b).Negative (eggs only,no spermadded) and posi- Seferiadis1977). In addition, the detectionof motilesperm in tive(conspeci ccrosses)controls were included for eachcross. light microscopicpreparations at ´ 400 or ´ 1000 magni cation Mitoticdivisions were present in all fertilized eggs, but not in was taken as beingevidence for the presenceof competent negative controls,and parthenogenesis doesnot occurin Fucus. sperm.Chemotaxis orsperm motility was not quanti ed. Reproductivesuccess of the crosseswas de nedas development DNA fromfresh ordried tissue was extracted as describedin to four-week-oldembryos. Coyer et al. (2002a).The following vemicrosatellite loci were The numbersof eggs peroogonium and the sizesof eggs were genotyped: FsA198,FsB113, FsB128, FsD39 and FsF4(Coyer quanti edin one individual of each Fe, female Fs and female et al. 2002a).ITS1 allelesand haplotypes ofchloroplast (rubisco hybrid. Batches of oogonia werecollected after releasefrom the spacer)and mitochondria( nad11)were determined by SSCP receptaclesand the numbersof cellsper oogonium were coun- analysis (Coyer et al. 2002b). Proc.R. Soc. Lond. B (2002) Hybridizationin FucusJ. A.Coyer andothers 1831 3 50 2 40 ) % 7 1 . 4 ( 2 ) s . i e 30 0 x . a s ( y t i s _ n 1 e 20 d _2 _2 _1 0 1 2 10 axis 1 (19.8 %) Figure 3. Two-dimensional FCA of all eld individuals. The 0 _ _
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