Estudos filogenômicos e morfológicos integrados em Gigartinales: resolvendo o clado mais desafiador em Rhodophyta

Abstract

Gigartinales is one of the most species-rich orders within Rhodophyta, with significant ecological and economic importance. Ecologically, it contributes to habitat formation, serves as a food source for marine organisms, and participates in ocean biogeochemical cycles. Economically, it provides bioactive compounds used in the food, cosmetic, and pharmaceutical industries. Currently, 951 species distributed across 36 families are recognized. However, the morphological traits used to delimit taxa exhibit broad variation and are not exclusive to this clade, suggesting that the current circumscription of Gigartinales does not adequately reflect its evolutionary history. Furthermore, phylogenetic relationships among lineages show low support, especially in ancestral branches. Based on this complex taxonomic history, this study aimed to circumscribe Gigartinales using morphological and molecular evidence, proposing a taxonomic framework that reflects its evolution. A total of 57 species of Gigartinales and Peyssonneliales were sequenced, using specimens from historical collections and fresh samples preserved in silica gel. This yielded 37 complete mitochondrial genomes and 40 complete plastid genomes, providing 28 mitochondrial and 215 plastid genes used for phylogenetic construction. Additionally, 248 nuclear LSU gene (28S) sequences were obtained from GenBank, with three new LSU sequences generated in this study. Maximum likelihood analyses were conducted via the CIPRES Science Gateway, while alignments for synteny analyses were performed in Mauve, with gene gain and loss inferred using Dollo parsimony in COUNT. Five traits were selected for evolutionary analyses: habit, thallus form, growth type, procarp formation, and type of tetrasporangial division. Occurrence data for Gigartinales, sourced from GBIF and Algaebase, were used for biogeographic analyses, with the correlation between these databases tested using Pearson’s correlation coefficient. The results revealed that Gigartinales, with 100% support in organellar phylogenies, includes all sampled species of Peyssonneliales, representing the major genera of the family Peyssonneliaceae. Organellar phylogenies indicated inconsistencies in the placement of Gigartinaceae, Phylophoraceae, and Phacelocarpaceae, while the topology of the nuclear tree was congruent with the plastidial tree. These genomic phylogenies provided a robust framework for interpreting molecular events such as gene losses, gains, translocations, and inversions, as well as the evolution of morphological traits. Biogeographic analysis identified species richness hotspots along the Pacific coast of the United States, southern Australia, and Europe. Pearson’s correlation test revealed a significant positive relationship between GBIF and Algaebase data. Phylogenetic diversity metrics indicated distinct phylogenetic structures in Gigartinales communities despite similar species richness. These findings underscore the need for broader genetic sampling and well-resolved phylogenies to investigate relationships among red algal lineages. Furthermore, additional studies on macroalgal collections and digital metadata are essential to clarify ecological contributions and sampling biases in phylogenetic diversity patterns.