Resurrection of the Family Grateloupiaceae Emend. (Halymeniales, Rhodophyta) Based on a Multigene Phylogeny and Comparative Reproductive Morphology

Abstract

The marine red algal order Halymeniales currently includes two families, the Halymeniaceae and Tsengiaceae, and consist of 38 genera and about 358 species. Phylogenetic analyses on specific taxa of the order are common, but not comprehensive, leaving the many intra-ordinal relationships within the Halymeniales unresolved. To reassess the phylogeny of the Halymeniales, we conducted extensive phylogenetic analyses based on 207 rbcL sequences and multigene analyses (rbcL, psaA, psbA, cox1, and LSU) using 47 taxa from the order. The combined data set fully supports the monophyly of the Grateloupia sensu lato clade. Phylogenetic assessment of the reproductive structures in the order using the type of auxiliary cell ampullae, pericarp origin, and tetrasporangial development characters, supports a Grateloupia sensu lato clade distinct from the Halymeniaceae exemplified by the generitype Halymenia. As a result, we propose to reinstate the family Grateloupiaceae Schmitz based on the Grateloupia sensu lato clade and including Grateloupia and eight other genera: Dermocorynus, Mariaramirezia, Neorubra, Pachymeniopsis, Kintokiocolax, Phyllymenia, Prionitis, and Yonagunia. The emended Grateloupiaceae is distinguished from the Halymeniaceae by the following three characteristics; (i) simple unbranched and unilateral type of auxiliary cell ampullae, (ii) pericarp formed densely by the fusion of secondary medullary filaments from subcortical cells and lateral ampullary filaments from a fusion cell complex, (iii) tetrasporangia originating laterally from the outer cortex. The Halymeniales comprises the monophyletic Grateloupiaceae, Halymeniaceae sensu lato (which requires further study), and the Tsengiaceae.

Molecular study of the rare genus Neoabbottiella (Rhodophyta) reveals its assignment to the Halymeniaceae is incorrect

“…In this alga the gonimoblast is surrounded by thick genalatinous covering. In contrast, in the Halymeniales, the auxiliary cell is basal to a second-or third-order or intercalary in a first-order filament of auxiliary cell ampullae and it is visible in intact auxiliary cell branches; connecting filaments terminally fuse with an auxiliary cell; the gonimoblast initial cell develops from the auxiliary cell or auxiliary fusion cell; and the carposporophyte has a pericarp, which is formed by secondary medullary filaments and lateral ampullary filaments borne from an auxiliary fusion cell complex (Kawaguchi et al 2004;Gargiulo et al 2013;Manghisi et al 2014;Rodríguez-Prieto et al 2018Kim et al 2021). This comparison shows that Neoabbottiella is improperly assigned to Halymeniales on the basis of reproductive characteristics.…”

“…2018, 2022; Kim et al . 2021). This comparison shows that Neoabbottiella is improperly assigned to Halymeniales on the basis of reproductive characteristics.…”

“…This resulted in Neoabbottiella being assigned to the Halymeniaceae (order Halymeniales) (Schneider and Wynne 2007;Pisareva and Klochkova 2013;Guiry and Guiry 2023). Nevertheless, some features of the reproductive anatomy of Neoabbottiella, namely, the intercalary position of the auxiliary cell fourth from the distal end of the auxiliary branch and its indistinguishability before contact with the connecting filament, as well as the absence of a pericarp or involucre of elongated ampullary filaments around the gonimoblast (Perestenko 1975(Perestenko , 1994, clearly distinguish this genus from Halymeniaceae sensu lato (Chiang 1970;Kim et al 2021). This allows us to hypothesize that the assignment of Neoabbottiella to Halymeniales may be incorrect.…”