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

IF 2 4区 生物学 Q2 MARINE & FRESHWATER BIOLOGY
Raül Golo, Emma Cebrian, Pilar Díaz-Tapia, Petra Lucic, Razzy Hoffman, Alga Vergés
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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for providing photographs and resolving questions, as Marc Verlaque and Wilson Freshwater for his help in finding unpublished sequences.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]. 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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].
入侵的 Lophocladia 属(Rhodomelaceae,Rhodophyta)的系统发育分析揭示了 L. lallemandii 与 L. trichoclados 的同义,以及 L. kuetzingii 在东北大西洋的首次记录
摘要单纯依靠形态特征对红藻进行物种鉴定具有重要的挑战性。因此,分子信息的缺失往往掩盖了错误的识别、隐性多样性和引入的隐性物种。在Lophocladia属内,物种传统上是根据细微的形态特征来划分的。trichoclados和Lophocladia lallemandii在温暖和温带沿海地区被广泛记录,后者被认为是地中海的入侵物种。然而,这些物种之间的分子关系仍未被探索。为了弥补这一空白,我们对东北大西洋、地中海和红海的Lophocladia进行了全面的分类重新评估。通过对75个标本的分子和形态分析,在研究区确定了两个不同的Lophocladia类群。rbcL质体基因序列明确表明lallmandii和L. trichoclados是同源的。因此,我们提出L. lallemandii与L. trichoclados同义,具有命名优先权。本文首次在北大西洋Macaronesian地区报道了一种可能来自澳大利亚的引种L. kuetzingii。这一发现强调了扩大红藻DNA数据集的重要性,因为这样的努力大大提高了我们检测和辨别引入物种的能力。此外,这项研究强调了引入物种的分类学不确定性,即使是那些已经被归类为入侵物种的物种。分子工具揭示了Lophocladia lallemandii与L. trichoclados.L.同义。三爪鱼广泛分布于大西洋、地中海和红海。kuetzingii是在马卡罗尼亚地区发现的一种隐种引种。关键词:海藻bloomsCeramialescryptic introductionsinvasive speciesMacaronesiaMediterraneanrbcLRed Seataxonomy AcknowledgementsWe承认l . Le Gall她在a .路边援助的访问巴黎自然历史博物馆的标本(PC)和帕特里克•Froden谢谢植物博物馆的馆长标本(LD)促进了模式标本的照片。我们也感谢John M. Huisman提供照片和解决问题,以及Marc Verlaque和Wilson Freshwater帮助寻找未发表的序列。Razy Hoffman感谢Tal Perevolotsky从红海埃拉特的大学间研究所收集了三爪龙Lophocladia trichoclados标本。特拉维夫大学植物科学和食品安全学院也因其显微镜和相机的使用而受到认可。澳大利亚的一些标本是由霍尔斯沃思野生动物研究基金会资助的,它们的序列数据是在墨尔本大学的H. Verbruggen实验室生成的,得到了国家分类学研究基金(澳大利亚生物资源研究,RFL213-08)的财政支持。披露声明作者未报告潜在的利益冲突。以下补充材料可通过文章在线页面https://doi.org/10.1080/09670262.2023.2260443.Supplementary上的补充内容选项卡访问。基于rbcL基因进行系统发育重建的栉虫标本。根据区域将位置分开,并在括号之间表示精确位置。补充图S1本研究中使用的所有样本之间的相似性矩阵(使用百分比)。最深的颜色代表最大的相似性(约98.6%),最浅的颜色对应于L. kuetzingii(7-8%的差异)与L. trichoclados。kuetzingii样品间差异为99.2% ~ 100%。Haplodasya sp.作为外群。作者contributionsR。Golo:构思研究,进行实验室工作,参与数据集分析,撰写,手稿的关键修改,并最终批准发表;E. Cebrian:构思研究,参与数据集分析,承担项目管理和监督,对稿件进行关键性修改并最终批准发表;P. Diaz-Tapia:负责实验室工作,参与数据集分析,提供样本,参与文章审稿,对稿件进行关键性修改,并最终批准发表;P. Lucic:参与数据集分析,提供样本,参与文章审稿,对稿件进行关键性修改,最终批复发表;R。 Hoffman:参与数据集分析,提供样本,参与文章审稿,对稿件进行关键性修改,最终批复发表;A. vergs:构思研究,进行实验室工作,参与数据集分析,写作,承担项目管理和监督,对手稿进行关键修改,并最终批准发表。西班牙卫生部项目ANIMA [No. 1]提供了资金支持。CGL2016-76341-R, MINECO/FEDER, UE]和FoRestA,西班牙科学与创新部[资助/奖励号:pid2020 - 112985 gb - i00]。这项工作也得到了FPI资助[项目ANIMA, BES-2017-079907]给RG的支持。AV、RG和EC是医疗保险研究小组的成员[www.medrecover.org;2017 SGR 1521]。Pilar Díaz-Tapia得到了Xunta de Galicia [' Axudas de apoio <e:1> etapa de formación posdoutoral ' [grant ED481D/2017/011]的支持。本研究得到了克罗地亚科学基金会项目MAUD [IP-2018-01-9849]和Benthic NIS [IP-2019-04-6702]的部分支持。
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来源期刊
European Journal of Phycology
European Journal of Phycology 生物-海洋与淡水生物学
CiteScore
4.80
自引率
4.20%
发文量
37
审稿时长
>12 weeks
期刊介绍: The European Journal of Phycology is an important focus for the activities of algal researchers all over the world. The Editors-in-Chief are assisted by an international team of Associate Editors who are experts in the following fields: macroalgal ecology, microalgal ecology, physiology and biochemistry, cell biology, molecular biology, macroalgal and microalgal systematics, applied phycology and biotechnology. The European Journal of Phycology publishes papers on all aspects of algae, including cyanobacteria. Articles may be in the form of primary research papers and reviews of topical subjects. The journal publishes high quality research and is well cited, with a consistently good Impact Factor.
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