Species Boundaries and Global Biogeography of the Alexandrium Tamarense Complex (Dinophyceae)1
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J. Phycol. 43, 1329–1338 (2007) Ó 2007 Phycological Society of America DOI: 10.1111/j.1529-8817.2007.00420.x SPECIES BOUNDARIES AND GLOBAL BIOGEOGRAPHY OF THE ALEXANDRIUM TAMARENSE COMPLEX (DINOPHYCEAE)1 Emily L. Lilly2 University of Massachusetts Dartmouth, Biology II-330B, North Dartmouth, Massachusetts 02747, USA Kenneth M. Halanych Auburn University, Life Science Building, Auburn, Alabama 36849, USA and Donald M. Anderson Woods Hole Oceanographic Institution, MS #32, Woods Hole, Massachusetts 02543, USA Alexandrium catenella (Whedon et Kof.) Balech, Abbreviations: bp, base pair; ITS, internal tran- A. tamarense (M. Lebour) Balech, and A. fundyense scribed spacer; PSP, paralytic shellfish poisoning Balech comprise the A. tamarense complex, dinofla- gellates responsible for paralytic shellfish poisoning worldwide. The relationships among these morpho- Paralytic shellfish poisoning (PSP) is a potentially logically defined species are poorly understood, as fatal disorder caused by ingesting shellfish that con- are the reasons for increases in range and bloom tain high levels of neurotoxins called the saxitoxins. occurrence observed over several decades. This The parent compound, saxitoxin, and its congeners study combines existing data with new ribosomal are produced by phytoplankton and accumulated in DNA sequences from strains originating from the the tissues of filter-feeding shellfish (Taylor et al. six temperate continents to reconstruct the biogeog- 1995). Dinoflagellates of the genus Alexandrium are raphy of the complex and explore the origins of the most numerous and widespread saxitoxin pro- new populations. The morphospecies are examined ducers and are responsible for PSP blooms in sub- under the criteria of phylogenetic, biological, and arctic, temperate, and tropical locations (Taylor et al. morphological species concepts and do not to sat- 1995). The majority of toxic blooms have been caused isfy the requirements of any definition. It is recom- by the morphospecies A. catenella, A. tamarense, mended that use of the morphospecies appellations and A. fundyense (Cembella 1998), which together within this complex be discontinued as they imply comprise the A. tamarense species complex (Balech erroneous relationships among morphological vari- 1985). ants. Instead, five groups (probably cryptic species) Until 1970, PSP-causing dinoflagellates in the are identified within the complex that are supported A. tamarense complex were known only from Eur- on the basis of large genetic distances, 100% boot- ope, North America, and Japan (Hallegraeff 1993). strap values, toxicity, and mating compatibility. By 2000, A. tamarense complex cells had been docu- Every isolate of three of the groups that has been mented in the Northern and Southern hemispheres, tested is nontoxic, whereas every isolate of the adding South America, South Africa, Australia, the remaining two groups is toxic. These phylogenetic Pacific Islands, India, all of Asia, and the Mediterra- groups were previously identified within the A. tama- nean to the known range (Hallegraeff 1993, Abadie rense complex and given geographic designations et al. 1999, Vila et al. 2001a). Concomitant with this that reflected the origins of known isolates. For at substantial biogeographic expansion, the frequency least two groups, the geographically based names of toxic Alexandrium blooms has also greatly are not indicative of the range occupied by mem- increased (Anderson 1989, Hallegraeff 1993). bers of each group. Therefore, we recommend a Because of the serious human health and eco- simple group-numbering scheme for use until the nomic impacts associated with PSP, this alarming taxonomy of this group is reevaluated and new spe- increase has spurred the scientific community to cies are proposed. investigate its origins. Four main theories have been Key index words: Alexandrium; biogeography; cate- proposed for this expansion (Anderson 1989): nella; fundyense; paralytic shellfish poisoning; phy- (i) The increase is actually an artifact of increased logeny; tamarense; taxonomy monitoring efforts uncovering previously undetected populations. (ii) Toxic populations have spread within regions through natural means, including transport in currents followed by the deposition of a 1Received 14 June 2006. Accepted 26 July 2007. dormant cyst stage. (iii) Environmental change, 2Author for correspondence: e-mail [email protected]. 1329 1330 EMILY L. LILLY ET AL. including eutrophication and global warming, may bution is more limited, occurring mainly on the have caused toxic populations that were a normal, east coast of North America (Taylor 1984). but minor, component of native flora to bloom to Because the morphological differences are slight nuisance proportions. (iv) New populations have and multiple morphospecies can co-occur (Taylor been initiated by human-assisted dispersal mecha- 1984, Anderson et al. 1994), researchers have nisms, including ballast water transport and the searched for molecular evidence confirming or con- importation of contaminated shellfish seed stock. flicting with the morphospecies identifications. The The recognition of previously undetected popula- findings initially were confusing due to variation tions is possible because global awareness of HABs among geographic locations, supporting a distinc- has risen, and monitoring efforts have expanded tion between A. catenella and A. tamarense in Japan along with coastal fishing and aquaculture (Ander- (Sako et al. 1990, 1993, Adachi et al. 1994) but find- son 1989, Hallegraeff 1993). However, new popula- ing no clear differences in western or eastern North tions of A. tamarense and A. catenella have also been America and even uncovering morphological inter- detected in areas such as Thau Lagoon and Barce- mediates (Taylor 1984, Cembella and Taylor 1986, lona Harbor where established monitoring pro- Hayhome et al. 1989, Anderson et al. 1994). Addi- grams demonstrated a lack of these species prior tionally, sexual reproduction was observed between to their recent appearance (Abadie et al. 1999, Vila clonal isolates of A. tamarense and A. fundyense, et al. 2001a), and their subsequent spread (Penna which yielded viable progeny capable of sexually et al. 2005). producing an F2 generation (Anderson et al. 1994). Examples also can be found to support each of Each of these studies included multiple morpho- the remaining three hypotheses. For example, the species, but all isolates were from a limited geo- source of Alexandrium populations in Argentina is graphic region. In the mid-1990s, Scholin and unknown, but the spread of these organisms north- Anderson (1994, 1996) and Scholin et al. (1994, ward through Uruguay and Brazil is thought to be 1995) published a series of studies comparing DNA connected to the Malvinas current (Gayoso 2001, sequences from ribosomal genes for A. catenella, Persich et al. 2006). Human-assisted dispersal may A. tamarense, and A. fundyense strains from locations explain the appearance of A. catenella populations in eastern and western North America, Western Eur- in the Mediterranean (Lilly et al. 2002), and human ope, Japan, and Australia along with several ballast alteration of the environment may be allowing that water samples. Overall, these studies indicated that species to thrive and spread in its new habitat (Vila morphology is not a good indicator of evolutionary et al. 2001b). relationships within the A. tamarense complex. Information like this is available for very few Scholin et al. (1994) delineated five main phylo- A. tamarense populations, and much of the evidence genetic clades, which they named after the origin for other introductions is circumstantial (Gayoso of the majority of strains in each clade: North 2001, Vila et al. 2001b, Persich et al. 2006). Yet if we American, Western European, Temperate Asian, are to prevent further spread of A. tamarense–com- Tasmanian, and Tropical Asian. The fifth clade, plex cells, we must understand the causes for their Tropical Asian, consisted of a single sequence from current distribution. This undertaking requires isolate CU-13, which is now considered a member investigation into two avenues: taxonomy and DNA of a different species, A. tropicale Balech (Balech phylogeny. 1995, Lilly 2003). The Tasmanian clade also con- Unfortunately, taxonomy of the A. tamarense com- tained a single isolate. The North American clade plex is contentious, with some researchers believing contained examples of all three morphospecies, that the three morphologically defined species A. catenella, A. tamarense, and A. fundyense. In addi- (morphospecies), A. catenella, A. tamarense, and tion to strains from North America, this clade also A. fundyense, are true biological species (as defined contained the two A. tamarense strains that had been by Mayr 1982). However, others contend that the examined from Japan. The remaining strains from morphological variations are not indicative of Japan were all A. catenella, and their sequences fell shared genetic heritage and instead may be varia- into a separate phylogenetic group, the Temperate tions within a single species (Anderson et al. 1994, Asian. Scholin et al. 1995). The morphospecies are highly As yet, no consensus has been reached regarding similar in overall appearance, distinguished mainly the delineation of species within the A. tamarense by chain-forming ability, cell shape, and the pres- complex, but the work of Scholin et al. (1994) has ence or absence of a ventral pore between plates 1¢ highlighted the utility of DNA sequences for