Global phylogeny, biogeography, and evolution of the agarophyte family Gracilariaceae with key insights into broadly distributed and cultivated species

Abstract

This study investigates the global phylogeny, biogeography, and evolutionary history of Gracilariaceae, an ecologically and economically significant red algal family, with insights into cultivated and broadly distributed species. Using all available cox1 and rbcL DNA sequences and associated biogeographic data, we constructed the most comprehensive Gracilariaceae phylogeny and time-tree to date, mapping DNA-supported species distributions. Our dataset includes 161 Gracilariaceae lineages, of which 121 correspond to currently accepted species names. This dataset represents approximately 50 % of the currently described diversity within the family. However, considering all 161 lineages, our sampling covers approximately 66 % of the potential diversity represented by currently described species. Phylogenetic analyses resolved eight distinct clades, confirming the monophyly of Gracilaria, Gracilariopsis, and Melanthalia, but not Curdiea. Divergence time estimates place the Gracilariaceae crown group origin in the Jurassic (~170 Mya), with a Paleogene diversification burst. Global diversity hotspots occur in the tropical Central Indo-Pacific and Atlantic, followed by Northern Temperate regions. Approximately 73 % of species diversity is tropical, with 85 % concentrated in the Central Indo-Pacific and Atlantic. Biogeographic reconstructions suggest a Central Indo-Pacific origin for the order, followed by global dispersal and diversification hotspots in the same tropical regions. Macroevolutionary analyses reveal varying speciation patterns across clades, with the youngest, originating in the tropical Atlantic, exhibiting a notable speciation burst associated with flattened thallus morphology, suggesting a link between morphology and diversification. Geographic range restriction is typical in Gracilariaceae, with 84 % of species limited to a single longitudinal and 80 % to a single latitudinal region. Widely distributed species are exceptional and include previously documented introduced species. We identified 15 species with wide or disjunct distributions, detailing their geographic distribution and potential origins. Aquaculture poses invasion risks, as 10 of the 38 cultivated species exhibit broad or disjunct distributions, including previously documented cases of introduced species.