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Genetic approaches to exploring in situ marine phytoplankton assemblages have revealed previously unsuspected diversity at different taxonomic levels. However, the phylogenetic species concept has rarely been compared to classical morphologically based taxonomy, which forms the basis of most current ecological, physiological, and paleontological knowledge of phytoplankton. Here we use the coccolithophores as a case study to test the relationship between these two taxonomic approaches. Analysis of 217 coccolithophore LSU rDNA sequences and 729 specimens observed by light and electron microscopy obtained from three water samples (Atlantic Ocean, Pacific Ocean and Mediterranean Sea) demonstrated that parallel analysis of morphological and genetic data highlights limitations inherent to each approach. Combined morpho-genetic analyses increase the scope of description of the composition, richness and structure of natural coccolithophore communities. Overall, genetic determined diversity exceeded morphological determined diversity, which may partly reflect methodological biases, but also probably reflects cryptic speciation and/or the presence of lightly- or non-calcifying species (or life cycle stages) within the coccolithophore clade. Focusing on six coccolithophore family or order level subgroups, we show that the genetic diversity within established morphospecies varied significantly in different environments. Critically, we find that the divergence threshold at which phylospecies corresponded to morphospecies varied between different natural communities, a factor that may have important implications with respect to evaluation of diversity by metagenomics approaches.