https://orcid.org/0000-0002-5927-4570
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ABSTRACT
Cystoseira sensu lato (s.l.) – encompassing the genera Cystoseira sensu stricto (s.s.), Ericaria and Gongolaria – is a diverse group of forest-forming brown macroalgae endemic to the warm-temperate North-east Atlantic. These algae have immense biogeographic and ecological significance and have been experiencing recent regional declines. Most Cystoseira s.l. display important morphological plasticity and can be confused with similar species. Therefore, species boundaries, geographic ranges and phylogenetic affinities remain imprecise for most. In the face of persistent taxonomic difficulties, several authors underlined the necessity for new molecular-based approaches, but studies so far lacked representativity, resolution and standardization. To fill in these gaps, in this study we sequenced a comprehensive collection of Cystoseira s.l. spanning its entire North-east Atlantic range for a ~1200 bp cox1 barcode, and sequenced selected individuals representing major genetic entities for a few additional plastid markers. Phylogeographic, phylogenetic and species delimitation methods revealed 27 Molecular Operational Taxonomic Units, including unaccounted cryptic diversity, and elucidated with unprecedented resolution species compositions and phylogenetic relationships within each genus. Some entities within the lineages Cystoseira compressa/humilis, Ericaria brachycarpa/crinita, E. selaginoides and tophulose Gongolaria, as well as among free-living algae, conflicted with a priori taxonomic assignments, and required the redefinition, reinstatement and recognition of new taxa. For some, diagnostic mutations and biogeography were more useful for species identifications than morphological characters or conventional barcoding gaps. A few species showed narrow geographic ranges and others were the sole representatives of their respective lineages. Several sister-species showed Atlantic vs Mediterranean complementary ranges. Phylogenetic signal of cox1 was nevertheless insufficient to confidently determine patterns of lineage splitting in several lineages and species complexes and did not improve significantly with additional plastid markers. We discuss novel systematics and biogeography insights considering the advantages and shortcomings of the barcoding approach employed, and how this comprehensive baseline study can be expanded to address multiple questions still left unanswered.
HIGHLIGHTS
Identification of major genetic entities of Cystoseira s.s., Ericaria and Gongolaria.
A comprehensive reference cox1 barcode library for Cystoseira s.l.
Updated systematics and biogeography of Cystoseira s.l.
Acknowledgements
The authors thank the invaluable help of many colleagues and friends who contributed with samples and helped in sampling campaigns, including Annalisa Falace, Cristina Linares, Aschwin Engelen, Begoña Martínez Crego, Buga Berković, Cátia Freitas, Cristina Paulino, Christophe Vieira, Duarte Frade, Duarte Neiva, Francisco Fernandes, Gonçalo Silva, Tânia Aires, João Tiago Tavares, Karim Erzini, Luis Barreto, Neusa Martins, Nuri Max Steinmann, Paulo Catry, Peter Wirtz, Rita Jacinto, Roberto Buonomo, Diego Kurt Kersting, Jana Verdura and Jorge Santamaría. We thank Marta Valente for sequencing work.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Supplementary material
The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2022.2126894
Supplementary table S1. PCR amplification conditions.
Supplementary table S2. List of cox1 sequences of Cystoseira, Ericaria and Gongolaria spp. from Genbank used in the present study.
Supplementary table S3. Submitted Genbank sequences and data-sets (last four columns) used in the different analyses.
Supplementary figure S1. Maximum-Likelihood cox1 phylogenetic tree of Cystoseira s.l. and related genera.
Supplementary figure S2. Morphology of free-living Cystoseira s.l. from southern Iberia and northern Morocco.
Supplementary figure S3. General morphology and polymorphism of Ericaria brachycarpa s.s.
Supplementary figure S4. General morphology of Ericaria crinita s.l. from Crete.
Supplementary figure S5. General morphology and polymorphism of Gongolaria elegans from Catalonia.
Supplementary figure S6. General morphology of Gongolaria sp. 2.
Supplementary figure S7. General morphology and polymorphism of “Gongolaria sp. 1” MOTU.
Supplementary figure S8. Best “single-gene” Maximum Likelihood phylogenetic trees of Cystoseira s.s.
Supplementary figure S9. Best “single-gene” Maximum Likelihood phylogenetic trees of Ericaria.
Supplementary figure S10. Best “single-gene” Maximum Likelihood phylogenetic trees of Gongolaria.
Author contributions
JN, GAP, EAS conceived the study; JN, RB, AM, PC, DMF, EB, BS, DS, EN, JS, JV, MM, SSS, GAP, EAS collected the samples; JN, MM, SSS obtained sequences and conducted genetic analyses; MDG conducted the taxonomic review; JN drafted the manuscript with important contributions from RB, EB, DS, FT, SSS, MDG and EAS. JN, PA, EB, BS, DS, FT, AI, EAS provided funds for sampling campaigns and/or laboratory analyses. All authors read, edited, and approved the final manuscript.