Molecular phylogeny of Boninia (Platyhelminthes: Polycladida), with description of a new species from the Pacific coasts of Panama
Aoi Tsuyuki A B * , Jon Norenburg C , Francesca Leasi D and Marco Curini-Galletti EA
B
C
D
E
Abstract
Mesopsammic polyclad members in the family Boniniidae have attracted attention in terms of their evolutionary shifts of microhabitat and their unique morphology such as a pair of pointed tentacles extending from the anterolateral margins and prostatoid organs harbouring stylets. Here, we establish a new species of this family as Boninia panamensis sp. nov. from the Pacific coasts of Panama, based on its morphological characteristics of (i) four cerebral and 61–80 marginal eyespots, (ii) two prostatoid organs located anterior and posterior to the penis papilla, and (iii) two uterine canals departing from the anterior part of the Lang’s vesicle. We also report Boninia cf. uru from Hawai’i, USA, based on its morphological identity with B. uru from Okinawa, Japan, along with their genetic distances for the partial cytochrome c oxidase subunit I (COI) sequences, which were beyond the range of intraspecific differences observed in congeners in this study. Boninia oaxaquensis is also reported from Panama as a new locality for the species. Involving the above-mentioned three species sequenced herein, we reconstructed molecular phylogenetic trees of Boninia based on the four gene markers (18S rDNA, 28S rDNA, 16S rDNA and COI). Our phylogenetic trees indicated the synapomorphy within the genus Boninia of the small numbers of stylets (2–4) and the connection route of the uterine canals to the Lang’s vesicle. The results also showed a characteristic distribution pattern in which pairs of species in distinct lineages occurred sympatrically with different microhabitats, as observed in Boninia uru and Boninia yambarensis in Okinawa and B. panamensis sp. nov. and B. oaxaquensis in Panama. In addition, we discuss possible speciation pathways in this genus based on the tree topology.
ZooBank: urn:lsid:zoobank.org:pub:D414BACD-C14A-4B34-8AF9-7ACBA28F46D0
Keywords: biogeography, circumtropical distribution, Cotylea, Eastern Pacific Barrier, histology, interstitial, nomenclature, taxonomy.
References
Akaike H (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716-723.
| Crossref | Google Scholar |
Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F (2004) Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20, 407-415.
| Crossref | Google Scholar | PubMed |
Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N, Bamber R, Barber A, Bartsch I, Berta A, Błażewicz-Paszkowycz M, Bock P, Boxshall G, Boyko CB, Brandão SN, Bray RA, Bruce NL, Cairns SD, Chan T-Y, Cheng L, Collins AG, Cribb T, Curini-Galletti M, Dahdouh-Guebas F, Davie PJF, Dawson MN, De Clerck O, Decock W, De Grave S, de Voogd NJ, Domning DP, Emig CC, Erséus C, Eschmeyer W, Fauchald K, Fautin DG, Feist SW, Fransen CHJM, Furuya H, Garcia-Alvarez O, Gerken S, Gibson D, Gittenberger A, Gofas S, Gómez-Daglio L, Gordon DP, Guiry MD, Hernandez F, Hoeksema BW, Hopcroft RR, Jaume D, Kirk P, Koedam N, Koenemann S, Kolb JB, Kristensen RM, Kroh A, Lambert G, Lazarus DB, Lemaitre R, Longshaw M, Lowry J, Macpherson E, Madin LP, Mah C, Mapstone G, McLaughlin PA, Mees J, Meland K, Messing CG, Mills CE, Molodtsova TN, Mooi R, Neuhaus B, Ng PKL, Nielsen C, Norenburg J, Opresko DM, Osawa M, Paulay G, Perrin W, Pilger JF, Poore GCB, Pugh P, Read GB, Reimer JD, Rius M, Rocha RM, Saiz-Salinas JI, Scarabino V, Schierwater B, Schmidt-Rhaesa A, Schnabel KE, Schotte M, Schuchert P, Schwabe E, Segers H, Self-Sullivan C, Shenkar N, Siegel V, Sterrer W, Stöhr S, Swalla B, Tasker ML, Thuesen EV, Timm T, Todaro MA, Turon X, Tyler S, Uetz P, van der Land J, Vanhoorne B, van Ofwegen LP, van Soest RWM, Vanaverbeke J, Walker-Smith G, Walter TC, Warren A, Williams GC, Wilson SP, Costello MJ (2012) The magnitude of global marine species diversity. Current Biology 22, 2189-2202.
| Crossref | Google Scholar | PubMed |
Bock S (1923) Boninia, a new polyclad genus from the Pacific. Nova Acta Regiae Societatis Scientiarum Upsaliensis (4) 6, 1-32.
| Google Scholar |
Briggs JC (1961) The east pacific barrier and the distribution of marine shore fishes. Evolution 15, 545-554.
| Crossref | Google Scholar |
Briggs JC (1974) Operation of zoogeographic barriers. Systematic Biology 23, 248-256.
| Crossref | Google Scholar |
Chernomor O, von Haeseler A, Minh BQ (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65, 997-1008.
| Crossref | Google Scholar | PubMed |
Curini-Galletti M, Campus P (2007) Boninia neotethydis sp. nov. (Platyhelminthes: Polycladida: Cotylea)—the first lessepsian flatworm. Journal of the Marine Biological Association of the United Kingdom 87, 435-442.
| Crossref | Google Scholar |
Curini-Galletti M, Artois T, Domenico MD, Fontaneto D, Jondelius U, Jörger KM, Leasi F, Martínez A, Norenburg JL, Sterrer W, Todaro MA (2020) Contribution of soft-bodied meiofaunal taxa to Italian marine biodiversity. The European Zoological Journal 87, 369-384.
| Crossref | Google Scholar |
Dittmann IL, Cuadrado D, Aguado MT, Noreña C, Egger B (2019) Polyclad phylogeny persists to be problematic. Organisms Diversity & Evolution 19, 585-608.
| Crossref | Google Scholar |
Du Bois-Reymond Marcus E, Marcus E (1968) Polycladida from Curaçao and faunistically related regions. Studies on the fauna of Curaçao and other Caribbean Islands 101, 1-133.
| Google Scholar |
Faubel A (1984) The Polycladida, Turbellaria. Proposal and establishment of a new system. Part II. The Cotylea. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 81, 189-259.
| Google Scholar |
Hyman LH (1955) Some polyclad flatworms from the West Indies and Florida. Proceedings of the United States National Museum 104, 115-150.
| Google Scholar |
Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20, 1160-1166.
| Crossref | Google Scholar |
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870-1874.
| Crossref | Google Scholar | PubMed |
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35, 1547-1549.
| Crossref | Google Scholar | PubMed |
Laidlaw FF (1906) On the marine fauna of the Cape Verde Islands, from collections made in 1904 by Mr C. Crosslan—the polyclad Turbellaria. Proceedings of the Zoological Society of London 2, 705-719.
| Google Scholar |
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695-1701.
| Crossref | Google Scholar | PubMed |
Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772-773.
| Crossref | Google Scholar |
Laumer CE, Giribet G (2014) Inclusive taxon sampling suggests a single, stepwise origin of ectolecithality in Platyhelminthes. Biological Journal of the Linnean Society 111, 570-588.
| Crossref | Google Scholar |
Leasi F, Andrade SCdS, Norenburg J (2016) At least some meiofaunal species are not everywhere. Indication of geographic, ecological and geological barriers affecting the dispersion of species of Ototyphlonemertes (Nemertea, Hoplonemertea). Molecular Ecology 25, 1381-1397.
| Crossref | Google Scholar | PubMed |
Litvaitis MK, Bolaños DM, Quiroga SY (2019) Systematic congruence in Polycladida (Platyhelminthes, Rhabditophora): are DNA and morphology telling the same story? Zoological Journal of the Linnean Society 186, 865-891.
| Crossref | Google Scholar |
Minh BQ, Nguyen MAT, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30, 1188-1195.
| Crossref | Google Scholar | PubMed |
Newman LJ, Cannon LRG (1995) The importance of the fixation of colour, pattern and form in tropical Pseudocerotidae (Platyhelminthes, Polycladida). Hydrobiologia 305, 141-143.
| Crossref | Google Scholar |
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268-274.
| Crossref | Google Scholar | PubMed |
Oya Y, Kajihara H (2017) Description of a new Notocomplana species (Platyhelminthes: Acotylea), new combination and new records of Polycladida from the northeastern Sea of Japan, with a comparison of two different barcoding markers. Zootaxa 4282, 526-542.
| Crossref | Google Scholar |
Oya Y, Kajihara H (2020) Molecular phylogenetic analysis of Acotylea (Platyhelminthes: Polycladida). Zoological Science 37, 271-279.
| Crossref | Google Scholar | PubMed |
Prudhoe S (1944) On some polyclad turbellarians from the Cayman Islands. Annals and Magazine of Natural History 11, 322-334.
| Google Scholar |
Ramos-Sánchez M, Bahia J, Bastida-Zavala JR (2020) Five new species of cotylean flatworms (Platyhelminthes: Polycladida: Cotylea) from Oaxaca, southern Mexican Pacific. Zootaxa 4819, 4819.
| Crossref | Google Scholar | PubMed |
Romero-Torres M, Treml EA, Acosta A, Paz-García DA (2018) The Eastern Tropical Pacific coral population connectivity and the role of the Eastern Pacific Barrier. Scientific Reports 8, 9354.
| Crossref | Google Scholar | PubMed |
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
| Crossref | Google Scholar | PubMed |
Scarpa F, Cossu P, Sanna D, Lai T, Norenburg JL, Curini-Galletti M, Casu M (2015) An 18S- and 28S-based clock calibration for marine Proseriata (Platyhelminthes). Journal of Experimental Marine Biology and Ecology 463, 22-31.
| Crossref | Google Scholar |
Sonnenberg R, Nolte AW, Tautz D (2007) An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Frontiers in Zoology 4, 6.
| Crossref | Google Scholar |
Soutullo P, Cuadrado D, Noreña C (2021) First study of the Polycladida (Rhabditophora, Platyhelminthes) from the Pacific Coast of Costa Rica. Zootaxa 4964, 363-381.
| Crossref | Google Scholar | PubMed |
Steenwyk JL, Buida TJ, Li Y, Shen X-X, Rokas A (2020) ClipKIT: a multiple sequence alignment trimming software for accurate phylogenomic inference. PLoS Biology 18, e3001007.
| Crossref | Google Scholar | PubMed |
Tsuyuki A, Oya Y, Jimi N, Kajihara H (2020) Description of Pericelis flavomarginata sp. nov. (Polycladida: Cotylea) and its predatory behavior on a scaleworm. Zootaxa 4894, 403-412.
| Crossref | Google Scholar |
Tsuyuki A, Oya Y, Kajihara H (2022) Reversible shifts between interstitial and epibenthic habitats in evolutionary history: molecular phylogeny of the marine flatworm family Boniniidae (Platyhelminthes: Polycladida: Cotylea) with descriptions of two new species. PLoS ONE 17, e0276847.
| Crossref | Google Scholar | PubMed |
Tsuyuki A, Oya Y, Jimi N, Hookabe N, Fujimoto S, Kajihara H (2023a) Theama japonica sp. nov., an interstitial polyclad flatworm showing a wide distribution along Japanese Coasts. Zoological Science 40, 262-272.
| Crossref | Google Scholar |
Tsuyuki A, Oya Y, Kajihara H (2023b) A new species of slender flatworm in the genus Eucestoplana and a record of E. cf. cuneata (Platyhelminthes, Polycladida) from the Okinawa Islands, Japan, with an inference of their phylogenetic positions within Cestoplanidae. Zoosystematics and Evolution 99, 363-373.
| Crossref | Google Scholar |