Molecular evolution of the Alexandrium tamarense ‘species complex’ (Dinophyceae): dispersal in the North American and West Pacific regions

Abstract

Hypotheses concerning the molecular evolution, population structure and dispersal of the toxic dinoflagellates Alexandrium tamarense (Lebour) Balech, A. catenella (Whedon et Kofoid) Balech and A. fundyense Balech (the ‘tamarensis species complex’) are examined in light of previous reports that compared their small and large-subunit ribosomal RNA gene (SSU and LSU rDNA) sequences. Forty-eight cultures from North America, western Europe, Japan, Australia and Thailand were analysed by a restriction fragment length polymorphism (RFLP) assay of SSU rDNA, and 34 of those by sequencing a fragment of LSU rDNA. Results indicate that the tamarensis species complex comprises at least 5 genetically distinct evolutionary lineages (‘ribotypes’) whose phylogenetic relationships reflect geographic populations, not morphospecies. We believe this pattern reveals a monophyletic radiation from an ancestor that included or gave rise to multiple morphotypes. Accumulated mutations in descendants’ SSU and LSU rDNA are suggested to reflect the prolonged geographic isolation and independent evolution of distinct populations. Novel SSU rDNA data are presented in support of this hypothesis. Given the proposed evolutionary framework and other historical considerations, we interpret the genetic diversity of Japanese A. tamarense/catenella as indicative of dispersed populations from genetically distinct sources. The possibility that A. catenella was introduced to Australia from an Asian source is also considered. In both cases, however, rDNA data alone are insufficient to distinguish whether this occurred thousands of years ago by natural immigrations or as a result of recent human activity (ballast water transport or relays of shellfish stocks). The uncertainty of dispersal timing stems from the relatively slow rate at which rDNA evolves and lack of fossil evidence. Ballast water samples show that viable toxigenic Alexandrium cysts have undergone human-assisted transoceanic transport, illustrating how a region could be ‘seeded’ with genetically distinct A. tamarense and A. catenella from a variety of regional populations.