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Comprehensive phylogenetic analyses of the Ruppia maritima complex focusing on taxa from the Mediterranean

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Abstract

Recent molecular phylogenetic studies reported high diversity of Ruppia species in the Mediterranean. Multiple taxa, including apparent endemics, are known from that region, however, they have thus far not been exposed to phylogenetic analyses aimed at studying their relationships to taxa from other parts of the world. Here we present a comprehensive phylogenetic analyses of the R. maritima complex using data sets composed of DNA sequences of the plastid genome, the multi-copy nuclear ITS region, and the low-copy nuclear phyB gene with a primary focus on the Mediterranean representatives of the complex. As a result, a new lineage, “Drepanensis”, was identified as the seventh entity of the complex. This lineage is endemic to the Mediterranean. The accessions included in the former “Tetraploid” entity were reclassified into two entities: an Asia–Australia–Europe disjunct “Tetraploid_α” with a paternal “Diploid” origin, and a European “Tetraploid_γ” originating from a maternal “Drepanensis” lineage. Another entity, “Tetraploid_β”, is likely to have been originated as a result of chloroplast capture through backcrossing hybridization between paternal “Tetraploid_α” and maternal “Tetraploid_γ”. Additional discovery of multiple tetraploidizations as well as hybridization and chloroplast capture at the tetraploid level indicated that hybridization has been a significant factor in the diversification of Ruppia.

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Acknowledgments

The authors thank Dr. P. Garcia-Murillo (Seville, Spain), Dr. S. Sciandrello (Sicily, Italy), Mr. S. Mifsud (Malta), Dr. H. Freitag (Kassel, Germany), Dr. S. R. Yadav (Kolhapur, India), Dr. J. J. Orth (Virginia, USA), Dr. H. J. Cho (Mississippi, USA), and Dr. S. W. L. Jacobs (Sydney, Australia) for their help with field research and Drs. D. Potter (California, USA) and P. B. Pelser (Christchurch, NZ) for revising the draft version of this manuscript.

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  1. Yu Ito

    Present address: School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, 8020, New Zealand

Authors and Affiliations

  1. Department of Biology, University of Saskatchewan, 112 Science Pl., Saskatoon, S7N 5E2, Canada

    Yu Ito

  2. Botanical Gardens, Graduate School of Science, The University of Tokyo, 3-7-1 Hakusan, Bunkyo-ku, Tokyo, 112-0001, Japan

    Tetsuo Ohi-Toma & Jin Murata

  3. Tsukuba Botanical Garden, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, 305-0005, Japan

    Norio Tanaka

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  1. Yu Ito
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  2. Tetsuo Ohi-Toma
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  3. Jin Murata
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Correspondence to Norio Tanaka.

Appendices

Appendix 1

The 1st data set for Fig. 1. The taxonomic grouping of Triest and Sierens (2013); OTUs; GenBank accessions: psbA–trnH, and ITS; sample origins; Voucher specimens; haplotype of Triest and Sierens (2010); and ITS type of Triest and Sierens (2013). Note that Hybrid Spain has no specific haplotype and ITS accessions in Triest and Sierens (2010, 2013); only haplotype and ITS type are shown. Samples from Triest and Sierens (2010, 2013) are indicated by underlines. DNA accessions obtained in the present study are shown with asterisks.

“ R. maritima ”—R. maritima S. Africa: JN113274, JN113282 + JN113285; S. Africa; LT-RH-20 (BRVU); haplotype d; ITS-a. R. maritima France: JN113269, JN113282 + JN113285; France; LT-R-678 (BRVU); haplotype d; ITS-a. R. maritima Finland: JN113272, JN113282 + JN113285; Finland; LT-R-2540 (BRVU); haplotype d; ITS-a. R. maritima B: AB728718*, AB728734*; Anatom Island, Vanuatu; TNS9516725 (TNS). R. maritima B’: AB728719*, AB728735*; Yuhong, Sanya, Hainan, China; YI00743 (TNS). R. maritima B’’: AB728720*, AB728736*; Maharashtra, India; YI01209 (TNS). R. maritima B’’’: AB728737*, AB728721*; Grand Bay, Gulf of Mexico, Jackson, Mississippi, USA; YI01233 (TNS). R. maritima C: AB728722*, AB728738*; Chesapeake Bay, Maryland, USA; YI00958 (TNS). R. maritima D: AB728723*, AB728739*; Cape Breton Island, Nova Scotia, Canada; CAN521697 (SAP).

“ R. cirrhosa _I”—R. cirrhosa Italy: JN113271, JN113282 + JN113285; Italy; LT-R-1325 (BRVU); haplotype e; ITS-a. R. cirrhosa Spain_I: JN113270, JN113282 + JN113285; Spain; LT-R-199 (BRVU); haplotype e; ITS-a. R. cirrhosa Egypt: JN113273, JN113282 + JN113285; Egypt; LT-RH-18 (BRVU); haplotype e; ITS-a. R. maritima E: AB728725*, AB728741*; Montecollina Bore, c. 218 km NE Lyndhurst, Strzelecki Track, South Australia, Australia; SJ9694 (TI, TNS, NSW). R. maritima E’: AB728726*, AB728742*, AB728743*; Shiokawa River, Okinawa, Japan; YI00754 (TNS). R. maritima H: AB728727*, AB728744*; Canatilla, Huelva, Spain; YI01552 (TNS).

“ R. cirrhosa _II”—R. cirrhosa Greece: JN113267, JN113280 + JN113283; Greece; LT-R-750 (BRVU); haplotype b; ITS-b. R. cirrhosa Spain_II: JN113268, JN113280 + JN113283; Spain; LT-R-2328 (BRVU); haplotype b; ITS-b. R. cirrhosa A: AB728730*, AB728748*, AB728749*; Skye Island, U.K.; YI01299 (TNS). R. maritima F: AB728731*, AB728750*; Dubrovnik, Croatia; YI00878 (TNS). R. maritima K: AB728732*, AB728751*; Vendicari Natural Reserve, Noto, Sicily, Italy; YI01571 (TNS). R. maritima L: AB728733*, AB728752*; Bonba, Huelva, Spain; YI01549 (TNS).

“ R. drepanensis ”—R. drepanensis Spain: JN113266, JN113281 + JN113284; Spain; LT-R-91 (BRVU); haplotype a; ITS-c. R. cirrhosa B: AB728724*, AB728740*; Donana National Park, Sevilla, Spain; YI01567 (TNS).

“cp-capture”—Hybrid Spain: Spain; haplotype b; ITS-a. R. maritima I: AB728728*, AB728745*; Gozo Island, Malta; YI01491 (TNS). R. maritima J: AB728729*, AB728746*, AB728747*; Morgerra Salt Marsh, Marzanemi, Sicily, Italy; YI01575 (TNS).

Appendix 2

The 2nd data set for Fig. 2. The entities of the R. maritima complex; OTUs; GenBank accessions: matK, rbcL, rpoB, rpoC1, and phyB (a = partially obtained sequences); sample origins; Voucher specimens. DNA accessions obtained in the present study are shown with asterisks.

“Diploid”—R. maritima B: AB507905, AB507865, AB507945, AB507985, AB508028; Anatom Island, Vanuatu; TNS9516725 (TNS). R. maritima B’: AB507914, AB507874, AB507954, AB507994, AB508037; Yuhong, Sanya, Hainan, China; YI00743 (TNS). R. maritima B’’: AB507910, AB507870, AB507950, AB507990, AB508033; Maharashtra, India; YI01209 (TNS). R. maritima B’’’: AB507908, AB507868, AB507948, AB507988, AB508031; Grand Bay, Gulf of Mexico, Jackson, Mississippi, USA; YI01233 (TNS). R. maritima C: AB507911, AB507871, AB507951, AB507991, AB508034; Chesapeake Bay, Maryland, USA; YI00958 (TNS). R. maritima D: AB507907, AB507867, AB507947, AB507987, AB508030; Cape Breton Island, Nova Scotia, Canada; CAN521697 (SAP).

“Drepanensis”—R. cirrhosa B: AB728682*, AB728688*, AB728694*, AB728700*, AB728706*, AB728707*; Donana National Park, Sevilla, Spain; YI01567 (TNS).

“Filifolia”—R. maritima G; AB534779, AB534787, AB534793, AB534799, AB534808, AB534809; Port Stephens, West Falkland, Falklands, UK; YI01251 (TNS).

“Occidentalis”—R. polycarpa B: AB507937, AB507897, AB507977, AB508017, AB508073; Redberry Lake, Saskatchewan, Canada; YI01264 (TNS).

“Tetraploid_α”—R. maritima E: AB507919, AB507879, AB507959, AB507999, aAB508046, aAB508047; Montecollina Bore, c. 218 km NE Lyndhurst, Strzelecki Track, South Australia, Australia; SJ9694 (TI, TNS, NSW). R. maritima E’: AB507924, AB507884, AB507964, AB508004, AB508056, AB508057; Shiokawa River, Okinawa, Japan; YI00754 (TNS). R. maritima H: AB728683*, AB728689*, AB728695*, AB728701*, AB728708*, AB728709*; Canatilla, Huelva, Spain; YI01552 (TNS).

“Tetraploid_β”—R. maritima I: AB728684*, AB728690*, AB728696*, AB728702*, AB728710*, AB728711*; Gozo Island, Malta; YI01491 (TNS). R. maritima J: AB728685*, AB728691*, AB728697*, AB728703*, AB728747*, AB728712*, AB728713*; Morgerra Salt Marsh, Marzanemi, Sicily, Italy; YI01575 (TNS).

“Tetraploid_γ”—R. cirrhosa A: AB507925, AB507885, AB507965, AB508005, AB508058, AB508059*; Skye Island, U.K.; YI01299 (TNS). R. maritima F: AB507915, AB507875, AB507955, AB507995, AB508038, AB508039; Dubrovnik, Croatia; YI00878 (TNS). R. maritima K: AB728686*, AB728692*, AB728698*, AB728704*, AB728714*, AB728715*; Vendicari Natural Reserve, Noto, Sicily, Italy; YI01571 (TNS). R. maritima L: AB728687*, AB728693*, AB728699*, AB728705*, AB728716*, AB728717*; Bonba, Huelva, Spain; YI01549 (TNS).

“Utahian”—R. maritima A; AB507928, AB507888, AB507968, AB508008, AB508064; Salt Lake City, Utah, U.S.A.; YI01274 (TNS).

R. polycarpa S. Mason—R. polycarpa A: AB507938, AB507898, AB507978, AB508018, AB508074; Coila Creek, S Moruya, New South Wales, Australia; SJ9719 (NSW).

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Ito, Y., Ohi-Toma, T., Murata, J. et al. Comprehensive phylogenetic analyses of the Ruppia maritima complex focusing on taxa from the Mediterranean. J Plant Res 126, 753–762 (2013). https://doi.org/10.1007/s10265-013-0570-6

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