Phylogenetic analysis of invasive genus Lophocladia (Rhodomelaceae, Rhodophyta) reveals synonymy of L. lallemandii with L. trichoclados and first record of L. kuetzingii in the NE Atlantic
Raül Golo, Emma Cebrian, Pilar Díaz-Tapia, Petra Lucic, Razzy Hoffman, Alga Vergés
{"title":"Phylogenetic analysis of invasive genus <i>Lophocladia</i> (Rhodomelaceae, Rhodophyta) reveals synonymy of <i>L. lallemandii</i> with <i>L. trichoclados</i> and first record of <i>L. kuetzingii</i> in the NE Atlantic","authors":"Raül Golo, Emma Cebrian, Pilar Díaz-Tapia, Petra Lucic, Razzy Hoffman, Alga Vergés","doi":"10.1080/09670262.2023.2260443","DOIUrl":null,"url":null,"abstract":"ABSTRACTSpecies identification in red algae poses significant challenges when relying solely on morphological characteristics. Consequently, the absence of molecular information often conceals misidentifications, cryptic diversity and introduced cryptic species. Within the genus Lophocladia, species have traditionally been delineated based on subtle morphological traits. Lophocladia trichoclados and Lophocladia lallemandii have been extensively documented in warm and temperate coastal regions, with the latter recognized as an invasive species in the Mediterranean. However, the molecular relationship between these species remains unexplored. To address this gap, a comprehensive taxonomic reevaluation of Lophocladia was conducted in the NE Atlantic, Mediterranean Sea and Red Sea. Through combined molecular and morphological analyses of 75 specimens, two distinct taxa of Lophocladia were identified within the study area. Sequences of the rbcL plastid gene unequivocally demonstrated that L. lallemandii and L. trichoclados are conspecific. Consequently, we propose the synonymization of L. lallemandii with L. trichoclados, which has nomenclatural priority. We report L. kuetzingii, a potentially introduced species from Australia, for the first time in the Macaronesian region of the North Atlantic. This finding underscores the importance of expanding red algal DNA datasets, as such efforts significantly enhance our ability to detect and discern introduced species. Additionally, this research highlights the existence of taxonomic uncertainties surrounding introduced species, even among those already classified as invasive.highlights Molecular tools reveal the synonymy of Lophocladia lallemandii with L. trichoclados.L. trichoclados is a widely distributed species in the Atlantic, Mediterranean and Red Sea.L. kuetzingii is detected as a cryptic introduced species in the Macaronesian region.KEYWORDS: Algal bloomsCeramialescryptic introductionsinvasive speciesMacaronesiaMediterraneanrbcLRed Seataxonomy AcknowledgementsWe acknowledge L. Le Gall for her assistance during A. Vergés’ visit to the Herbarium of the Natural History Museum Paris (PC) and thank Patrik Frödén as curator of the Botanical Museum herbarium (LD) who facilitated the pictures of type specimens. We also thank John M. Huisman for providing photographs and resolving questions, as Marc Verlaque and Wilson Freshwater for his help in finding unpublished sequences. Razy Hoffman acknowledges Tal Perevolotsky for collecting specimens of Lophocladia trichoclados from the Interuniversity Institution in Eilat, Red Sea. The School of Plant Sciences and Food Security of Tel Aviv University is also acknowledged for the use of their microscopes and cameras. Some of the Australian collections were possible through funding from the Holsworth Wildlife Research Endowment and their sequence data were generated in the H. Verbruggen laboratory at the University of Melbourne, through financial support of a National Taxonomy Research Grant (Australian Biological Resources Study, RFL213-08).Disclosure statementNo potential conflict of interest was reported by the author(s).Supplementary informationThe following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2023.2260443.Supplementary table S1. Lophocladia specimens used in phylogenetic reconstructions based on the rbcL gene. The localities are separated according to the region and the precise location is indicated between brackets.Supplementary fig. S1. Similarity matrix (using percentage) between all samples used in the present study. Darkest colours represent maximum similitude (>98.6% of similitude between Lophocladia trichoclados), and lightest colours correspond to L. kuetzingii (7-8% of differences) compared with L. trichoclados. Between L. kuetzingii samples the differences range from 99.2 to 100%. Haplodasya sp. was used as an outgroup.Author contributionsR. Golo: conceived the study, performed the laboratory work, participated in the analysis of the dataset, writing, critical revision of the manuscript and gave final approval for publication; E. Cebrian: conceived the study, participated in the analysis of the dataset, undertook project administration and supervision, critical revision of the manuscript and gave final approval for publication; P. Diaz-Tapia: performed the laboratory work, participated in the analysis of the dataset, provided samples and participated in the review of the article, critical revision of the manuscript and gave final approval for publication; P. Lucic: participated in the analysis of the dataset, provided samples and participated in the review of the article, critical revision of the manuscript and gave final approval for publication; R. Hoffman: participated in the analysis of the dataset, provided samples and participated in the review of the article, critical revision of the manuscript and gave final approval for publication; A. Vergés: conceived the study, performed the laboratory work, participated in the analysis of the dataset, writing, undertook project administration and supervision, critical revision of the manuscript and gave final approval for publication.Additional informationFundingFinancial support has been provided by Spanish Ministry Project ANIMA [No. CGL2016-76341-R, MINECO/FEDER, UE] and FoRestA, Spanish Ministry of Science and Innovation [Grant/Award No. PID2020-112985GB-I00]. This work was also supported by a FPI grant [project ANIMA, BES-2017-079907] to RG. AV, RG and EC are members of the MedRecover Research Group [www.medrecover.org; 2017 SGR 1521]. Pilar Díaz-Tapia received support from Xunta de Galicia [‘Axudas de apoio á etapa de formación posdoutoral’ [grant ED481D/2017/011]. This research was partially supported by the Croatian Science Foundation projects MAUD [IP-2018-01-9849] and Benthic NIS [IP-2019-04-6702].","PeriodicalId":2,"journal":{"name":"ACS Applied Bio Materials","volume":null,"pages":null},"PeriodicalIF":4.6000,"publicationDate":"2023-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"ACS Applied Bio Materials","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1080/09670262.2023.2260443","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"MATERIALS SCIENCE, BIOMATERIALS","Score":null,"Total":0}
引用次数: 0
Abstract
ABSTRACTSpecies identification in red algae poses significant challenges when relying solely on morphological characteristics. Consequently, the absence of molecular information often conceals misidentifications, cryptic diversity and introduced cryptic species. Within the genus Lophocladia, species have traditionally been delineated based on subtle morphological traits. Lophocladia trichoclados and Lophocladia lallemandii have been extensively documented in warm and temperate coastal regions, with the latter recognized as an invasive species in the Mediterranean. However, the molecular relationship between these species remains unexplored. To address this gap, a comprehensive taxonomic reevaluation of Lophocladia was conducted in the NE Atlantic, Mediterranean Sea and Red Sea. Through combined molecular and morphological analyses of 75 specimens, two distinct taxa of Lophocladia were identified within the study area. Sequences of the rbcL plastid gene unequivocally demonstrated that L. lallemandii and L. trichoclados are conspecific. Consequently, we propose the synonymization of L. lallemandii with L. trichoclados, which has nomenclatural priority. We report L. kuetzingii, a potentially introduced species from Australia, for the first time in the Macaronesian region of the North Atlantic. This finding underscores the importance of expanding red algal DNA datasets, as such efforts significantly enhance our ability to detect and discern introduced species. Additionally, this research highlights the existence of taxonomic uncertainties surrounding introduced species, even among those already classified as invasive.highlights Molecular tools reveal the synonymy of Lophocladia lallemandii with L. trichoclados.L. trichoclados is a widely distributed species in the Atlantic, Mediterranean and Red Sea.L. kuetzingii is detected as a cryptic introduced species in the Macaronesian region.KEYWORDS: Algal bloomsCeramialescryptic introductionsinvasive speciesMacaronesiaMediterraneanrbcLRed Seataxonomy AcknowledgementsWe acknowledge L. Le Gall for her assistance during A. Vergés’ visit to the Herbarium of the Natural History Museum Paris (PC) and thank Patrik Frödén as curator of the Botanical Museum herbarium (LD) who facilitated the pictures of type specimens. We also thank John M. Huisman for providing photographs and resolving questions, as Marc Verlaque and Wilson Freshwater for his help in finding unpublished sequences. Razy Hoffman acknowledges Tal Perevolotsky for collecting specimens of Lophocladia trichoclados from the Interuniversity Institution in Eilat, Red Sea. The School of Plant Sciences and Food Security of Tel Aviv University is also acknowledged for the use of their microscopes and cameras. Some of the Australian collections were possible through funding from the Holsworth Wildlife Research Endowment and their sequence data were generated in the H. Verbruggen laboratory at the University of Melbourne, through financial support of a National Taxonomy Research Grant (Australian Biological Resources Study, RFL213-08).Disclosure statementNo potential conflict of interest was reported by the author(s).Supplementary informationThe following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2023.2260443.Supplementary table S1. Lophocladia specimens used in phylogenetic reconstructions based on the rbcL gene. The localities are separated according to the region and the precise location is indicated between brackets.Supplementary fig. S1. Similarity matrix (using percentage) between all samples used in the present study. Darkest colours represent maximum similitude (>98.6% of similitude between Lophocladia trichoclados), and lightest colours correspond to L. kuetzingii (7-8% of differences) compared with L. trichoclados. Between L. kuetzingii samples the differences range from 99.2 to 100%. Haplodasya sp. was used as an outgroup.Author contributionsR. Golo: conceived the study, performed the laboratory work, participated in the analysis of the dataset, writing, critical revision of the manuscript and gave final approval for publication; E. Cebrian: conceived the study, participated in the analysis of the dataset, undertook project administration and supervision, critical revision of the manuscript and gave final approval for publication; P. Diaz-Tapia: performed the laboratory work, participated in the analysis of the dataset, provided samples and participated in the review of the article, critical revision of the manuscript and gave final approval for publication; P. Lucic: participated in the analysis of the dataset, provided samples and participated in the review of the article, critical revision of the manuscript and gave final approval for publication; R. Hoffman: participated in the analysis of the dataset, provided samples and participated in the review of the article, critical revision of the manuscript and gave final approval for publication; A. Vergés: conceived the study, performed the laboratory work, participated in the analysis of the dataset, writing, undertook project administration and supervision, critical revision of the manuscript and gave final approval for publication.Additional informationFundingFinancial support has been provided by Spanish Ministry Project ANIMA [No. CGL2016-76341-R, MINECO/FEDER, UE] and FoRestA, Spanish Ministry of Science and Innovation [Grant/Award No. PID2020-112985GB-I00]. This work was also supported by a FPI grant [project ANIMA, BES-2017-079907] to RG. AV, RG and EC are members of the MedRecover Research Group [www.medrecover.org; 2017 SGR 1521]. Pilar Díaz-Tapia received support from Xunta de Galicia [‘Axudas de apoio á etapa de formación posdoutoral’ [grant ED481D/2017/011]. This research was partially supported by the Croatian Science Foundation projects MAUD [IP-2018-01-9849] and Benthic NIS [IP-2019-04-6702].