Insights into the phylogenetic position and phylogeography of the monospecific skink-parasite genus Neoentomelas (Nematoda: Rhabditida: Rhabdiasidae), with special reference to the effects of the reproductive mode on the genetic diversity
Naoya Sata
A B * and Takafumi Nakano B
+ Author Affiliations
- Author Affiliations
A Meguro Parasitological Museum, Meguro-ku, Tokyo 153-0064, Japan.
B Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan.
Invertebrate Systematics 36(1) 36-47 https://doi.org/10.1071/IS21026
Submitted: 7 April 2021 Accepted: 14 November 2021 Published: 5 January 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
Neoentomelas asatoi Hasegawa, 1989 is a parasitic nematode that infests only the scincid lizard Ateuchosaurus pellopleurus (Hallowell, 1861) that inhabits the forest floor in the Northern and Central Ryukyu Archipelago, Japan. As a member of Rhabdiasidae, the reproductive mode of N. asatoi is characterised by the alternation of the protandrous hermaphroditic mode and gonochoristic mode throughout the life cycle. The intrafamily phylogenetic position and intraspecific diversity of this nematode species were inferred by molecular phylogenetic analyses. The results revealed the phylogenetic distinctiveness of Neoentomelas Hasegawa, 1989 in Rhabdiasidae that supports the unique generic status of Neoentomelas within the family. The intraspecific phylogenetic analyses of N. asatoi revealed a minor concordant phylogenetic pattern with the host and mosaic geographic arrangement of the major clades that was discordant with the host. The analyses and distribution pattern of subclades suggested that this geographic arrangement can be explained by at least three dispersal events and subsequent switching to indigenous host populations. Colonisation events might be promoted by the high establishment rate of new populations stemming from the parthenogenesis-like reproduction mode of N. asatoi. This study demonstrated that reproductive modes can affect the intraspecific genetic diversity of parasites.
Keywords: Ateuchosaurus pellopleurus, endoparasite, generic status, Japan, Neoentomelas asatoi, reproductive mode, Rhabdiasidae, Ryukyu Archipelago.
References
Anderson RC (2000) ‘Nematode parasites of vertebrates: their development and transmission’, 2nd edn. (CABI Publishing: Wallingford, UK)Badets, M, Whittington, I, Lalubin, F, Allienne, J-F, Maspimby, J-L, Bentz, S, Du Preez, LH, Barton, D, Hasegawa, H, Tandon, V, Imkongwapang, R, Ohler, A, Combes, C, and Verneau, O (2011). Correlating early evolution of parasitic platyhelminths to Gondwana breakup. Systematic Biology 60, 762–781.
| Correlating early evolution of parasitic platyhelminths to Gondwana breakup.Crossref | GoogleScholarGoogle Scholar | 21856629PubMed |
Baker, MR (1980). Revision of Entomelas Travassos, 1930 (Nematoda: Rhabdiasidae) with a review of genera and family. Systematic Parasitology 1, 83–90.
| Revision of Entomelas Travassos, 1930 (Nematoda: Rhabdiasidae) with a review of genera and family.Crossref | GoogleScholarGoogle Scholar |
Blasco-Costa, I, and Poulin, R (2013). Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 1316–1322.
| Host traits explain the genetic structure of parasites: a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 23866918PubMed |
Bursey, CR, Goldberg, SR, and Telford, SR (2005). Plagiorchis taiwanensis (Digenea: Plagiorchiidae), Kurilonema markovi (Nematoda: Rhabdiasidae) and other helminthes in Eumeces latiscutatus (Scincidae) and Takydromus tachydromoides (Lacertidae) from Japan. Comparative Parasitology 72, 234–240.
| Plagiorchis taiwanensis (Digenea: Plagiorchiidae), Kurilonema markovi (Nematoda: Rhabdiasidae) and other helminthes in Eumeces latiscutatus (Scincidae) and Takydromus tachydromoides (Lacertidae) from Japan.Crossref | GoogleScholarGoogle Scholar |
Casiraghi, M, Bain, O, Guerrero, R, Martin, C, Pocacqua, V, Gardner, SL, Franceschi, A, and Bandi, C (2004). Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. International Journal for Parasitology 34, 191–203.
| Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution.Crossref | GoogleScholarGoogle Scholar | 15037105PubMed |
Clement, M, Posada, D, and Crandall, KA (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
| TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 11050560PubMed |
Duméril AMC, Bibron G (1839) ‘Erpétologie Générale, ou, Histoire Naturalle Compléte des Reptiles, V.’ (Imprimeurs de l’Universite Royale de France: Paris, France)
Falk, BG, and Perkins, SL (2013). Host specificity shapes population structure of pinworm parasites in Caribbean reptiles. Molecular Ecology 22, 4576–4590.
| Host specificity shapes population structure of pinworm parasites in Caribbean reptiles.Crossref | GoogleScholarGoogle Scholar | 23848187PubMed |
Fitzinger LJ (1843) ‘Systema reptilium. Fasciculus primus Amblyglossae.’ (Braumüller et Seidel: Wien, German Confederation)
Furukawa, M, and Fujitani, T (2014). Comparative study on Pleistocene paleogeographic maps of Ryukyu Arc. Bulletin of the Faculty of Science University of the Ryukyus 98, 1–8.
Greer, AE, and Shea, GM (2000). A major new head scale character in non-lygosomine scincid lizards. Journal of Herpetology 34, 629–634.
| A major new head scale character in non-lygosomine scincid lizards.Crossref | GoogleScholarGoogle Scholar |
Hallowell, E (1861). Report upon the Reptilia of the North Pacific exploring expedition, under command of Capt. John Rogers, U.S.N. Proceedings Academy of Natural Sciences of Philadelphia 12, 480–510.
Hasegawa, H (1985). Helminth parasites of reptiles from Okinawa, Japan. The Biological Magazine Okinawa 23, 1–11.
Hasegawa, H (1989). Neoentomelas asatoi gen. et sp. n. (Nematoda: Rhabdiasidae) and Hedruris miyakoensis sp. n. (Nematoda: Hedruridae) from skinks of the Ryukyu Archipelago, Japan. Proceedings of the Helminthological Society of Washington 56, 145–150.
Hasegawa, H (1990). Helminths collected from amphibians and reptiles on Amami-oshima Island, Japan. Memoirs of the National Science Museum (Tokyo) 23, 83–92.
Hasegawa, H (1992). Parasitic helminths collected from amphibians and reptiles on Kume-jima Island, Okinawa, Japan. The Biological Magazine Okinawa 30, 7–13.
Hasegawa, H, and Iwatsuki, N (1984). Helminth fauna of tree lizard, Japarula polygonata in Okinawa Prefecture, Japan. Akamata 2, 18–26.
Haukisalmi, V, Hardman, LM, Fedorov, VB, Hoberg, EP, and Henttonen, H (2016). Molecular systematics and Holarctic phylogeography of cestodes of the genus Anoplocephaloides Baer, 1923 s. s. (Cyclophyllidae, Anoplocephalidae) in lemmings (Lemmus, Synaptomys). Zoologica Scripta 45, 88–102.
| Molecular systematics and Holarctic phylogeography of cestodes of the genus Anoplocephaloides Baer, 1923 s. s. (Cyclophyllidae, Anoplocephalidae) in lemmings (Lemmus, Synaptomys).Crossref | GoogleScholarGoogle Scholar |
Ikeda, H, Nishikawa, M, and Sota, T (2012). Loss of flight promotes beetle diversification. Nature Communications 3, 648.
| Loss of flight promotes beetle diversification.Crossref | GoogleScholarGoogle Scholar | 22337126PubMed |
Karve, JN (1930). Some parasitic nematodes of frogs and toads. Annals of Tropical Medicine and Parasitology 24, 481–491.
| Some parasitic nematodes of frogs and toads.Crossref | GoogleScholarGoogle Scholar |
Katoh, K, and Standley, DM (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar | 23329690PubMed |
Kisel, Y, and Barraclough, TG (2010). Speciation has a spatial scale that depends on levels of gene flow. American Naturalist 175, 316–334.
| Speciation has a spatial scale that depends on levels of gene flow.Crossref | GoogleScholarGoogle Scholar |
Koehler, AVA, Hoberg, EP, Dokuchaev, NE, Tranbenkova, NA, Whitman, JA, Nagorsen, DW, and Cook, JA (2009). Phylogeography of a Holarctic nematode, Soboliphyme baturini, among mustelids: climate change, episodic colonization, and diversification in a complex host–parasite system. Biological Journal of the Linnean Society. Linnean Society of London 96, 651–663.
| Phylogeography of a Holarctic nematode, Soboliphyme baturini, among mustelids: climate change, episodic colonization, and diversification in a complex host–parasite system.Crossref | GoogleScholarGoogle Scholar |
Kuzmin, YI (2013). Review of Rhabdiasidae (Nematoda) from the Holarctic. Zootaxa 3639, 1–76.
| Review of Rhabdiasidae (Nematoda) from the Holarctic.Crossref | GoogleScholarGoogle Scholar |
Kuzmin, YI, and Sharpilo, VP (2002). Rare and locally distributed helminth species of Palearctic: Kurilonema markovi (Nematoda, Rhabdiasidae), the lung parasite of the Japanese five-lined skink, Eumeces latiscutatus (Reptilia, Sauria, Scincidae). Vestnik Zoologii 36, 61–64.
Kuzmin, YI, and Tkach, VV (2011). Description of a new species of Kurilonema (Nematoda: Rhabdiasidae) from lungs of the skink Sphenomorphus abdictus aquilonius (Reptilia: Squamata: Scincidae) in the Philippines. The Journal of Parasitology 97, 506–512.
| Description of a new species of Kurilonema (Nematoda: Rhabdiasidae) from lungs of the skink Sphenomorphus abdictus aquilonius (Reptilia: Squamata: Scincidae) in the Philippines.Crossref | GoogleScholarGoogle Scholar |
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T, and 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.
| PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Leigh, JW, and Bryant, D (2015). POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.
| POPART: full-feature software for haplotype network construction.Crossref | GoogleScholarGoogle Scholar |
Linkem, CW, Diesmos, AC, and Brown, RM (2011). Molecular systematics of the Philippine forest skinks (Squamata: Scincidae: Sphenomorphus): testing morphological hypotheses of interspecific relationships. Zoological Journal of the Linnean Society 163, 1217–1243.
| Molecular systematics of the Philippine forest skinks (Squamata: Scincidae: Sphenomorphus): testing morphological hypotheses of interspecific relationships.Crossref | GoogleScholarGoogle Scholar | 32336789PubMed |
Makino, T, Okamoto, T, Kurita, K, Nakano, T, and Hikida, T (2020). Origin and intraspecific diversification of the scincid lizard Ateuchosaurus pellopleurus with implications for historical island biogeography of the Central Ryukyus of Japan. Zoologischer Anzeiger 288, 1–10.
| Origin and intraspecific diversification of the scincid lizard Ateuchosaurus pellopleurus with implications for historical island biogeography of the Central Ryukyus of Japan.Crossref | GoogleScholarGoogle Scholar |
Messing J (1983) New M13 vectors for cloning. In ‘Methods in enzymology recombinant DNA, Part C Vol. 101’. (Eds R Wu, L Grossman, K Moldave) pp. 20–78. (Academic Press: New York, NY, USA)
Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A, and Lanfear, R (2020). IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534.
| IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era.Crossref | GoogleScholarGoogle Scholar | 32011700PubMed |
Okamoto T (2017) Historical biogeography of the terrestrial reptiles of Japan: a comparative analysis of geographic ranges and molecular phylogenies. In ‘Species diversity of animals in Japan’. (Eds M Motokawa, H Kajihara) pp. 135–163. (Springer Japan KK: Tokyo, Japan)
Osozawa, S, Shinjo, R, Armid, A, Watanabe, Y, Horiguchi, T, and Wakabayashi, J (2012). Palaeogeographic reconstruction of the 1.55 Ma synchronous isolation of the Ryukyu islands, Japan, and Taiwan and inflow of the Kuroshio warm current. International Geology Review 54, 1369–1388.
| Palaeogeographic reconstruction of the 1.55 Ma synchronous isolation of the Ryukyu islands, Japan, and Taiwan and inflow of the Kuroshio warm current.Crossref | GoogleScholarGoogle Scholar |
Ota, H (1998). Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications. Researches on Population Ecology 40, 189–204.
| Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications.Crossref | GoogleScholarGoogle Scholar |
Ota, H, Miyaguni, H, and Hikida, T (1999). Geographic variation in the endemic skink, Ateuchosaurus pellopleurus from the Ryukyu Archipelago. Journal of Herpetology 33, 106–118.
| Geographic variation in the endemic skink, Ateuchosaurus pellopleurus from the Ryukyu Archipelago.Crossref | GoogleScholarGoogle Scholar |
Peterson, MA, and Denno, RF (1998). The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects. American Naturalist 152, 428–446.
| The influence of dispersal and diet breadth on patterns of genetic isolation by distance in phytophagous insects.Crossref | GoogleScholarGoogle Scholar |
Prosser, SWJ, Velarde-Aguilar, MG, León-Règagnon, V, and Hebert, PDN (2013). Advancing nematode barcoding: a primer cocktail for the cytochrome c oxidase subunit I gene from vertebrate parasitic nematodes. Molecular Ecology Resources 13, 1108–1115.
| Advancing nematode barcoding: a primer cocktail for the cytochrome c oxidase subunit I gene from vertebrate parasitic nematodes.Crossref | GoogleScholarGoogle Scholar |
Pyron, R, Burbrink, FT, and Wiens, JJ (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Ecology and Evolution 13, 93.
| A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A, Drummond, AJ, Xie, D, Baele, G, and Suchard, MA (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
| Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA, and Huelsenbeck, JP (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Sands, AF, Apanaskevich, DA, Matthee, S, Horak, IG, and Matthee, CA (2017). The effect of host vicariance and parasite life history on the dispersal of the multi-host ectoparasite, Hyalomma truncatum. Journal of Biogeography 44, 1124–1136.
| The effect of host vicariance and parasite life history on the dispersal of the multi-host ectoparasite, Hyalomma truncatum.Crossref | GoogleScholarGoogle Scholar |
Sata, N (2015). Distribution of parasitic nematodes in Japan with host–parasite relationship of lizards of Plestiodon (Reptilia: Squamata: Scincidae). Comparative Parasitology 82, 17–24.
| Distribution of parasitic nematodes in Japan with host–parasite relationship of lizards of Plestiodon (Reptilia: Squamata: Scincidae).Crossref | GoogleScholarGoogle Scholar |
Sata, N (2018). Allopatric speciation of Meteterakis (Heterakoidea: Heterakidae), a highly dispersible parasitic nematode, in the East Asian islands. Parasitology International 67, 493–500.
| Allopatric speciation of Meteterakis (Heterakoidea: Heterakidae), a highly dispersible parasitic nematode, in the East Asian islands.Crossref | GoogleScholarGoogle Scholar | 29702259PubMed |
Shcherbak, NN, and Sharpilo, VP (1969). Data on taxonomy, ecology and parasitology of reptiles from the Kuril Islands. Communication I. Vestnik Zoologii 4, 18–25.
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M, and Kumar, S (2011). MEGA5: molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetic analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 21546353PubMed |
Telford SR (1997) ‘The ecology of a symbiotic community. Vol. 1.’ (Krieger: Malabar, FL, USA)
Thompson, JD, Higgins, DG, and Gibson, TJ (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |
Tkach, VV, Kuzmin, YI, and Snyder, SD (2014). Molecular insight into systematics, host associations, life cycles and geographic distribution of the nematode family Rhabdiasidae. International Journal for Parasitology 44, 273–284.
| Molecular insight into systematics, host associations, life cycles and geographic distribution of the nematode family Rhabdiasidae.Crossref | GoogleScholarGoogle Scholar | 24560917PubMed |
Travassos, L (1930). Pesquizas helminthologicas realisadas em Hamburgo: VII. notas sobre os Rhabdiasoidea Railliet, 1916: (Nematoda). Memorias do Instituto Oswaldo Cruz 24, 161–181.
| Pesquizas helminthologicas realisadas em Hamburgo: VII. notas sobre os Rhabdiasoidea Railliet, 1916: (Nematoda).Crossref | GoogleScholarGoogle Scholar |
Wickström, LM, Haukisalmi, V, Varis, S, Hantula, J, Fedorov, VB, and Henttone, H (2003). Phylogeography of the circumpolar Paranoplocephala arctica species complex (Cestoda: Anoplocephalidae) parasitizing collared lemmings (Dicrostonyx spp.). Molecular Ecology 12, 3359–3371.
| Phylogeography of the circumpolar Paranoplocephala arctica species complex (Cestoda: Anoplocephalidae) parasitizing collared lemmings (Dicrostonyx spp.).Crossref | GoogleScholarGoogle Scholar | 14629352PubMed |
