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Type Specimen Sequencing, Multilocus Analyses, and Species Delimitation Methods Recognize the Cosmopolitan Corallina Berteroi and Establish the Northern Japanese C

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Type Specimen Sequencing, Multilocus Analyses, and Species Delimitation Methods Recognize the Cosmopolitan Corallina Berteroi and Establish the Northern Japanese C J. Phycol. *, ***–*** (2021) © 2021 Phycological Society of America DOI: 10.1111/jpy.13202 TYPE SPECIMEN SEQUENCING, MULTILOCUS ANALYSES, AND SPECIES DELIMITATION METHODS RECOGNIZE THE COSMOPOLITAN CORALLINA BERTEROI AND ESTABLISH THE NORTHERN JAPANESE C. YENDOI SP. NOV. (CORALLINACEAE, RHODOPHYTA)1 Martha S. Calderon 2 Laboratorio de Ecosistemas Marinos Antarticos y Sub-antarticos (LEMAS), Universidad de Magallanes, Punta Arenas, Chile Instituto de Ecologıa y Biodiversidad (IEB), Santiago, Chile Danilo E. Bustamante Instituto de Investigacion para el Desarrollo Sustentable de Ceja de Selva (INDES-CES), Universidad Nacional Toribio Rodrıguez de Mendoza, Chachapoyas, Peru Department of Civil and Environmental Engineering (FICIAM), Universidad Nacional Toribio Rodrıguez de Mendoza, Chachapoyas, Peru Paul W. Gabrielson Biology Department and Herbarium, Coker Hall CB 3280, University of North Carolina, Chapel Hill, Chapel Hill, North Carolina 27599-3280, USA Patrick T. Martone Botany Department & Biodiversity Research Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada Katharine R. Hind Department of Biology, University of Victoria, PO Box 1700 Station CSC, Victoria, BC V8W 2Y2, Canada Soren R. Schipper Botany Department & Biodiversity Research Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada and Andres Mansilla Laboratorio de Ecosistemas Marinos Antarticos y Sub-antarticos (LEMAS), Universidad de Magallanes, Punta Arenas, Chile Instituto de Ecologıa y Biodiversidad (IEB), Santiago, Chile A partial rbcL sequence of the lectotype specimen temperate SW Atlantic (Falkland Islands), cold and of Corallina berteroi shows that it is the earliest warm temperate SE Pacific, NW Pacific and available name for C. ferreyrae. Multilocus species southern Australia. Also proposed is C. yendoi sp. delimitation analyses (ABGD, SPN, GMYC, bPTP, nov. from Hokkaido, Japan, which was recognized and BPP) using independent or concatenated COI, as distinct by 10 of the 13 species discrimination psbA, and rbcL sequences recognized one, two, or analyses, including the multilocus BPP. three species in this complex, but only with weak Key index words: Coralline algae; Corallina caespitosa; support for each species hypothesis. Conservatively, C. ferreyrae; C. melobesioides; C. pinnatifolia; multilo- we recognize a single worldwide species in this cus phylogeny; new species; species boundaries complex of what appears to be multiple, evolving populations. Included in this species, besides C. ferreyrae C. caespitosa ,are , the morphologically Species are a fundamental unit in biological C. melobesioides rbc distinct , and, based on a partial L research, yet species delimitation can be objectively C. pinnatifolia sequence of the holotype specimen, . challenging (Kuchta et al. 2016). Multilocus genetic Corallina berteroi C. officinalis, , not is the data are increasingly being used to delimit species cosmopolitan temperate species found thus far in and to identify distinct evolutionary lineages (Jack- the NE Atlantic, Mediterranean Sea, warm son et al. 2017). In addition, DNA-based methods temperate NW Atlantic and NE Pacific, cold delimit species using various strategies such as genetic distance (e.g., automated barcode gap dis- covery algorithm, ABGD; statistical parsimony, SPN), 1Received 25 May 2021. Accepted 13 July 2021. 2Author for correspondence: e-mail [email protected]. coalescence (e.g., generalized mixed Yule coales- Editorial Responsibility: M. Vis (Associate Editor) cent, GMYC; Poisson tree processes, PTP; Bayesian 1 2 MARTHA S. CALDERON ET AL. phylogenetics and phylogeography, BPP; and phylo- Mexico, Peru, and USA. Specimens were dried with a towel geographic inference using approximate likeli- and immediately placed in silica gel for morphological and hoods, PHRAPL), and genealogical concordance molecular analyses. Voucher specimens were deposited in the herbarium of the Universidad de Magallanes (LEMAS), (genealogical concordance phylogenetic species University of British Columbia (UBC), and University of recognition, GCPSR; Luo et al. 2018, Bustamante North Carolina-Chapel Hill (NCU); herbarium acronyms fol- et al. 2019b). These approaches have been used to low Index Herbariorum online (Thiers 2021). Quantitative delineate eukaryotic species and investigate diversifi- morpho-anatomical characters represent average values with cation processes (Carstens et al. 2013, Liu et al. standard deviation from approximately 30 measurements. 2015); lately these are being widely used on coral- Photographs were taken using the Leica MC170 camera attached to EZ4 Leica stereomicroscope (Leica Microsystem, line algae (Pardo et al. 2014, Torrano-Silva et al. Wetzlar, Germany). 2018, Costa et al. 2019, Pezzolesi et al. 2019, Twist Molecular procedures. DNA extraction and amplifications et al. 2019, Brodie et al. 2020). were performed at Universidad Nacional Toribio Rodriguez To date, studies of Corallina systematics using DNA de Mendoza (UNTRM), UBC, and University of North sequencing have focused primarily on resolving Carolina-Chapel Hill UNC-CH. At UNTRM genomic DNA was whether or not species belong in the genus and on extracted from ˜ 5 mg of dried algae ground in liquid nitro- € correctly applying names by sequencing type mate- gen using a NucleoSpin Plant II Kit (Macherey-Nagel, Duren, – Germany) according to the manufacturer’s protocol; at UNC- rial. For example, based on DNA sequence data CH genomic DNA from field-collected specimens was and despite morphological similarity to Corallina spe- extracted following the protocol in Gabrielson et al. (2011), cies – C. elongata was shown to belong in its own but modified for type specimens by following the guidelines genus, Ellisolandia (Hind and Saunders 2013). In in Hughey and Gabrielson (2012); at UBC genomic DNA was addition, the type species of three other genera extracted from field-collected specimens according to Saun- thought to be distinct based on morpho-anatomical ders (2008) with modifications from Saunders and McDevit characters, namely Yamadaia (Segawa 1955), Marginis- (2012). The primer pairs for amplification and sequencing at UNTRM were the newly design 133F (CGTATGGAAT- porum (Yendo 1902), and Pachyarthron (Manza 1937), TAGCWCAACCMGG) - 947R (GCTGCWGTAAAATAAG- were all shown by DNA sequencing to belong in CACGTGT) for COI, F1- R2 (Yoon et al. 2002) for psbA, and Corallina (Martone et al. 2012, Hind and Saunders F57- 897cR, F645- R1150 (Freshwater and Rueness 1994, Lin 2013, Hind et al. 2014). No morpho-anatomical char- et al. 2002, Torrano-Silva et al. 2014) for rbcL; at UNC-CH acter or suite of characters has proved diagnostic for primers for field collected material were the same for psbA, Corallina or for Ellisolandia. Sequencing type speci- and for rbcL were F57-R1150, F753-RrbcS (Freshwater and Rueness 1994) and for rbcL from type material F1152Cor- mens of 18th through mid-20th century historical R1308Cor (Gabrielson et al. 2011); at UBC primers for psbA species (e.g., C. officinalis [epitype], C. cretaceum [lec- were the same, for COI were GWSFn (LeGall and Saunders totype], and C. ferreyrae [isotype]) has been critical 2010) and GWSRx (Clarkston and Saunders 2013), and for for researchers to correctly apply these names (Bro- rbcL were F57-R1150K (Freshwater and Rueness 1994, Lind- die et al. 2013, Hind et al. 2014, Bustamante et al. strom et al. 2015) and F753-rbcLrevNEW (Freshwater and 2019a). Just as no morpho-anatomical characters Rueness 1994, Kucera and Saunders 2012). â have proved diagnostic at the generic rank for tribe Amplification at UNTRM used GoTaq Green Master Mix (Promega, Madison, WI, USA), preparing a 25 lL solution. Corallinoideae, likewise none have proved diagnostic This included 3 lL of total DNA solution, 0.5 lL of each for- for Corallina species. ward and reverse primer (10 pmol), 12.5 lL of master mix, Herein, we provide additional examples of the and 8.5 lL MilliQ water. Reaction were cycled in a T100TM necessity to sequence type specimens to apply names Thermal Cycler (Bio-Rad, Hercules, CA, USA) using the fol- and of the inadequacy of morpho-anatomical charac- lowing parameters: 94°C for 2 min, followed by 40 cycles of 94°C for 30s, 47°C for 60 s, and 72°C for 60 s, and a final ters to distinguish Corallina species. We show that C. ° berteroi (type locality: Chile) is the oldest available extension of 72 C for 10 min. PCR products were elec- trophoresed on 1% agarose gels, purified using the NucleoS- name for the Corallina species currently known as C. pin Gel and PCR clean-up kit (Macherey-Nagel, Duren,€ ferreyrae (type locality: Pucusana, Peru, including C. Germany) following the manufacturer’s instructions, and caespitosa [type locality: Devon, England]) and that C. then sequenced commercially (Macrogen, Seoul, Korea). pinnatifolia (type locality: California, USA) is also a Full-length forward and reverse strands were determined for junior synonym, as is the morpho-anatomically diver- all taxa, and the electropherograms were edited using the gent C. melobesioides (type locality: Izu, Japan) with an Chromas v1.45 software (McCarthy 1998). Amplification and cleaning of PCR products at UNC-CH followed Hughey et al. extensive base and unigeniculate uprights. We also (2001); sequencing and alignment followed Gabrielson et al. show the non-congruence of different markers for (2011). Amplification of PCR products at UBC followed Hind resolving the phylogenetic relationships among Coral- and Saunders (2013); sequencing was done
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