Spatiotemporal genetic structure of regional-scale Alexandrium catenella dinoflagellate blooms explained by extensive dispersal and environmental selection

Abstract

Paralytic Shellfish Poisoning (PSP) caused by the dinoflagellate Alexandrium catenella is a wellknown global syndrome that negatively impacts human health and fishery economies. Understanding the population dynamics and ecology of this species is thus important for identifying determinants of blooms and associated PSP toxicity. Given reports of extensive genetic heterogeneity in the toxicity and physiology of Alexandrium species, knowledge of genetic population structure in harmful algal species such as A. catenella can also facilitate the understanding of toxic bloom development and ecological adaptation. In this study we employed microsatellite markers to analyze multiple A. catenella strains isolated from several sub-regions in the Gulf of Maine (GoM) during summer blooms, to gain insights into the sources and dynamics of this economically important phytoplankton species. At least three genetically distinct clusters of A. catenella were identified in the GoM. Each cluster contained representatives from different subregions, highlighting the extent of connectivity and dispersal throughout the region. This shared diversity could result from cyst beds created by previous coastal blooms, thereby preserving the overall diversity of the regional A. catenella population. Rapid spatiotemporal genetic differentiation of A. catenella populations was observed in local blooms, likely driven by natural selection through environmental conditions such as silicate and nitrate/nitrite concentrations, emphasizing the role of short-term water mass intrusions and biotic processes in determining the diversity and dynamics of marine phytoplankton populations. Given the widespread intraspecific diversity of A. catenella in GoM and potentially elsewhere, harmful algal blooms will likely *

Host genotype structures the microbiome of a globally dispersed marine phytoplankton

“…Although phytoplankton drift freely across the global ocean with nearly unlimited dispersal and divide primarily asexually, they still possess clear genetic structure. Phytoplankton species are organized into genetically distinct populations that possess phenotypic trait variation, are associated with specific environmental conditions, and undergo large increases in abundance, known as blooms ( 19 – 23 ). Furthermore, genetically distinct phytoplankton populations persist on time scales of decades to centuries ( 23 , 24 ), providing ample opportunity for populations to develop specific relationships with other microbes.…”

Seasonal genotype dynamics of a marine dinoflagellate: Pelagic populations are homogeneous and as diverse as benthic seed banks

“…Previous studies on other Alexandrium species reported temporal (Alpermann et al, 2009 ; Richlen et al, 2012 ) and spatiotemporal (Dia et al, 2014 ; Gao et al, 2019 ) genetic intrabloom differentiation. These were probably driven by natural selection through environmental conditions, such as nutrient concentrations (Gao et al, 2019 ), but solid evidence for this hypothesis is lacking.…”

“…Previous studies on other Alexandrium species reported temporal (Alpermann et al, 2009 ; Richlen et al, 2012 ) and spatiotemporal (Dia et al, 2014 ; Gao et al, 2019 ) genetic intrabloom differentiation. These were probably driven by natural selection through environmental conditions, such as nutrient concentrations (Gao et al, 2019 ), but solid evidence for this hypothesis is lacking. Similarly, Rynearson et al ( 2006 ) speculate that environmental conditions (solar irradiance and silicic acid concentrations) regulate bloom dynamics of distinct diatom populations via selection.…”

“…Within the past few decades our understanding of phytoplankton evolution has changed fundamentally from the assumption that marine phytoplankton populations are panmictic—due to potentially high dispersibility and unlimited gene flow—to a more complex view of genetically differentiated populations. A growing body of literature suggests that phytoplankton populations can be temporally differentiated (Dia et al, 2014 ; Erdner et al, 2011 ; Gao et al, 2019 ; Godhe et al, 2016 ; Lebret et al, 2012 ; Richlen et al, 2012 ; Sassenhagen et al, 2015 , 2018 ; Sefbom et al, 2018 ) and geographically structured due to physical barriers and/or environmental gradients (Godhe et al, 2016 ; Postel et al, 2020 ; Sjöqvist et al, 2015 ; Tahvanainen et al, 2012 ). Genetic structure developing within relatively short timescales or geographical distances implies that evolution may happen rapidly, for example within a few hundred generations (Collins et al, 2014 ).…”

Patterns in Alpha and Beta Phytoplankton Diversity along a Conductivity Gradient in Coastal Mediterranean Lagoons

“…Under different circumstances, environmental homogeneity has been shown to generate biotic homogenization and thus, low beta diversity of biological communities, including phytoplankton [65]. In aquatic ecosystems, hydrological connectivity has been associated with environmental homogeneity and hence, with species dispersal and high shared diversity throughout a region [66][67][68]. Even though hydrological connectivity is supported for the five lagoons connected to Vistonikos Gulf by tidal canals, according to our analyses, instead of finding evidence of biotic homogenization (i.e., low beta diversity and low turnover), we calculated relatively high beta diversity for the entire monitoring period.…”