The role of progenesis in the diversification of the interstitial annelid lineage Psammodrilidae
Katrine Worsaae A D , Gonzalo Giribet B and Alejandro Martínez A CA Marine Biological Section, Department of Biology, University of Copenhagen Universitetsparken 4, 2100 Copenhagen, Denmark.
B Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA.
C Italian National Research Council, Institute of Ecosystem Study CNR-ISE, Largo Tonolli 50, 28922 Verbania, Italy.
D Corresponding author. Email: kworsaae@bio.ku.dk
Invertebrate Systematics 32(4) 774-793 https://doi.org/10.1071/IS17063
Submitted: 15 July 2018 Accepted: 3 March 2018 Published: 27 July 2018
Abstract
Psammodrilidae constitutes a family of understudied, nearly completely ciliated, small-sized annelids, whose systematic position in Annelida remains unsettled and whose internal phylogeny is here investigated for the first time. Psammodrilids possess hooked chaetae typical of macroscopic tube-dwelling semi-sessile annelids, such as Arenicolidae. Yet, several minute members resemble, with their conspicuous gliding by ciliary motion and vagile lifestyle, interstitial fauna, adapted to move between sand grains. Moreover, psammodrilids exhibit a range of unique features, for example, bendable aciculae, a collar region with polygonal unciliated cells, and a muscular pumping pharynx. We here present a combined phylogeny of Psammodrilidae including molecular and morphological data of all eight described species (two described herein as Psammodrilus didomenicoi, sp. nov. and P. norenburgi, sp. nov.) as well as four undescribed species. Ancestral character state reconstruction suggests the ancestor of Psammodrilidae was a semi-sessile larger form. Miniaturisation seems to have occurred multiple times independently within Psammodrilidae, possibly through progenesis, yielding small species with resemblance to a juvenile stage of the larger species. We find several new cryptic species and generally reveal an unexpected diversity and distribution of this small family. This success may be favoured by their adaptive morphology, here indicated to be genetically susceptible to progenesis.
Additional keywords: archiannelids, Meiofauna, regressive evolution, Spiralia, total evidence phylogeny.
References
Aguado, M. T., and San Martín, G. (2009). Phylogeny of the Syllidae (Polychaeta) based on morphological data. Zoologica Scripta 38, 379–402.| Phylogeny of the Syllidae (Polychaeta) based on morphological data.Crossref | GoogleScholarGoogle Scholar |
Anderson, C. L., Strope, C. L., and Moriyama, E. N. (2011). SuiteMSA: visual tools for multiple sequence alignment comparison and molecular sequence simulation. BMC Bioinformatics 12, 184.
| SuiteMSA: visual tools for multiple sequence alignment comparison and molecular sequence simulation.Crossref | GoogleScholarGoogle Scholar |
Andrade, S. C., Novo, M., Kawauchi, G. Y., Worsaae, K., Pleijel, F., Giribet, G., and Rouse, G. W. (2015). Articulating “archiannelids”: phylogenomics and annelid relationships, with emphasis on meiofaunal taxa. Molecular Biology and Evolution 32, 2860–2875.
| Articulating “archiannelids”: phylogenomics and annelid relationships, with emphasis on meiofaunal taxa.Crossref | GoogleScholarGoogle Scholar |
Bartolomaeus, T. (1995a). Structure and formation of the uncini in Pectinaria koreni, Pectinaria auricoma (Terebellida) and Spirorbis spirorbis (Sabellida): implications for annelid phylogeny and the position of the Pogonophora. Zoomorphology 115, 161–177.
| Structure and formation of the uncini in Pectinaria koreni, Pectinaria auricoma (Terebellida) and Spirorbis spirorbis (Sabellida): implications for annelid phylogeny and the position of the Pogonophora.Crossref | GoogleScholarGoogle Scholar |
Bartolomaeus, T. (1995b). Zur Ultrastruktur von Psammodrilus balanoglossoides: hypothesen zur Stellung der Psammodrilida innerhalb der Annelida. Microfauna Marina 10, 295–303.
Bartolomaeus, T., and Meyer, K. (1997). Morphogenesis and phylogenetic significance of hooked setae in Arenicolidae (Polychaeta, Annelida). Invertebrate Biology 116, 227–242.
| Morphogenesis and phylogenetic significance of hooked setae in Arenicolidae (Polychaeta, Annelida).Crossref | GoogleScholarGoogle Scholar |
Boaden, P. J. S. (1961). Littoral interstitial species from Anglesey representing three families new to Britain. Nature 191, 512.
| Littoral interstitial species from Anglesey representing three families new to Britain.Crossref | GoogleScholarGoogle Scholar |
Boaden, P. J. S. (1963). The interstitial fauna of some North Wales beaches. Journal of the Marine Biological Association of the United Kingdom 43, 79–96.
| The interstitial fauna of some North Wales beaches.Crossref | GoogleScholarGoogle Scholar |
Boaden, P. J. S. (1976). Soft meiofauna of sand from the delta region of the Rhine, Meuse and Scheldt. Netherlands Journal of Sea Research 10, 461–471.
| Soft meiofauna of sand from the delta region of the Rhine, Meuse and Scheldt.Crossref | GoogleScholarGoogle Scholar |
Boyer, S. L., Clouse, R. M., Benavides, L. R., Sharma, P., Schwendinger, P. J., Karunarathna, I., and Giribet, G. (2007). Biogeography of the world: a case study from cyphophthalmid Opiliones, a globally distributed group of arachnids. Journal of Biogeography 34, 2070–2085.
| Biogeography of the world: a case study from cyphophthalmid Opiliones, a globally distributed group of arachnids.Crossref | GoogleScholarGoogle Scholar |
Capa, M., Hutchings, P., Aguado, M. T., and Bott, N. I. (2011). Phylogeny of Sabellidae (Annelida) and relationships with other taxa inferred from morphology and multiple genes. Cladistics 27, 449–469.
| Phylogeny of Sabellidae (Annelida) and relationships with other taxa inferred from morphology and multiple genes.Crossref | GoogleScholarGoogle Scholar |
Capa, M., Parapar, J., and Hutchings, P. (2012). Phylogeny of Oweniidae (Polychaeta) based on morphological data and taxonomic revision of Australian fauna. Zoological Journal of the Linnean Society 166, 236–278.
| Phylogeny of Oweniidae (Polychaeta) based on morphological data and taxonomic revision of Australian fauna.Crossref | GoogleScholarGoogle Scholar |
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
| Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |
Crease, T. J., and Colbourne, J. K. (1998). The unusually long small-subunit ribosomal RNA of the crustacean, Daphnia pulex: sequence and predicted secondary structure. Journal of Molecular Evolution 46, 307–313.
| The unusually long small-subunit ribosomal RNA of the crustacean, Daphnia pulex: sequence and predicted secondary structure.Crossref | GoogleScholarGoogle Scholar |
Curini-Galletti, M., Artois, T., Delogu, V., De Smet, W. H., Fontaneto, D., Jondelius, U., Leasi, F., Martínez, A., Meyer-Wachsmuth, I., Nilsson, K. S., Tongiorgi, P., Worsaae, K., and Todaro, M. A. (2012). Patterns of diversity in soft-bodied meiofauna: dispersal ability and body size matter. PLoS One 7, e33801.
| Patterns of diversity in soft-bodied meiofauna: dispersal ability and body size matter.Crossref | GoogleScholarGoogle Scholar |
De Bivort, B. L., Clouse, R. M., and Giribet, G. (2010). A morphometrics‐based phylogeny of the temperate Gondwanan mite harvestmen (Opiliones, Cyphophthalmi, Pettalidae). Journal of Zoological Systematics and Evolutionary Research 48, 294–309.
| A morphometrics‐based phylogeny of the temperate Gondwanan mite harvestmen (Opiliones, Cyphophthalmi, Pettalidae).Crossref | GoogleScholarGoogle Scholar |
Di Domenico, M., Martínez, A., Lana, P., and Worsaae, K. (2013). Protodrilus (Protodrilidae, Annelida) from the southern and southeastern Brazilian coasts. Helgoland Marine Research 67, 733–748.
| Protodrilus (Protodrilidae, Annelida) from the southern and southeastern Brazilian coasts.Crossref | GoogleScholarGoogle Scholar |
Di Domenico, M., Martínez, A., Lana, P., and Worsaae, K. (2014). Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences. Molecular Phylogenetics and Evolution 75, 202–218.
| Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences.Crossref | GoogleScholarGoogle Scholar |
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
| MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar |
Eibye-Jacobsen, D., and Kristensen, R. M. (1994). A new genus and species of Dorvilleidae (Annelida, Polychaeta) from Bermuda, with a phylogenetic analysis of Dorvilleidae, Iphitimidae and Dinophilidae. Zoologica Scripta 23, 107–131.
| A new genus and species of Dorvilleidae (Annelida, Polychaeta) from Bermuda, with a phylogenetic analysis of Dorvilleidae, Iphitimidae and Dinophilidae.Crossref | GoogleScholarGoogle Scholar |
Farris, S. J., Albert, V. A., Källersjö, M., Lipscomb, D., and Kluge, A. G. (1996). Parsimony jackknifing outperforms neighbor-joining. Cladistics 12, 99–124.
| Parsimony jackknifing outperforms neighbor-joining.Crossref | GoogleScholarGoogle Scholar |
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Giribet, G. (2007). Efficient tree searches with available algorithms. Evolutionary Bioinformatics 3, 341–356.
Giribet, G., Vogt, L., Pérez González, A., Sharma, P., and Kury, A. B. (2010). A multilocus approach to harvestman (Arachnida: Opiliones) phylogeny with emphasis on biogeography and the systematics of Laniatores. Cladistics 26, 408–437.
| A multilocus approach to harvestman (Arachnida: Opiliones) phylogeny with emphasis on biogeography and the systematics of Laniatores.Crossref | GoogleScholarGoogle Scholar |
Giribet, G., Sharma, P. P., Benavides, L. R., Boyer, S. L., Clouse, R. M., De Bivort, B. L., Dimitrov, D., Kawauchi, G. Y., Murienne, J., and Schwendinger, P. J. (2012). Evolutionary and biogeographical history of an ancient and global group of arachnids (Arachnida: Opiliones: Cyphophthalmi) with a new taxonomic arrangement. Biological Journal of the Linnean Society. Linnean Society of London 105, 92–130.
| Evolutionary and biogeographical history of an ancient and global group of arachnids (Arachnida: Opiliones: Cyphophthalmi) with a new taxonomic arrangement.Crossref | GoogleScholarGoogle Scholar |
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
Hendriks, L., Broeckhoven, C., Vandenberghe, A., Peer, Y., and Wachter, R. (1988). Primary and secondary structure of the 18S ribosomal RNA of the bird spider Eurypelma californica and evolutionary relationships among eukaryotic phyla. European Journal of Biochemistry 177, 15–20.
| Primary and secondary structure of the 18S ribosomal RNA of the bird spider Eurypelma californica and evolutionary relationships among eukaryotic phyla.Crossref | GoogleScholarGoogle Scholar |
Higgins, R. P., and Thiel, H. (1988). ‘Introduction to the Study of Meiofauna.’ (Smithsonian Institution Press: Washington, DC, USA.)
Holthe, T. (1986). Evolution, systematics, and distribution of the Polychaeta Terebellomorpha, with a catalogue of the taxa and a bibliography. Gunneria 55, 1–236.
Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
| MrBayes: Bayesian inference of phylogeny.Crossref | GoogleScholarGoogle Scholar |
Katoh, K., Misawa, K., Kuma, K. I., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.
| MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.Crossref | GoogleScholarGoogle Scholar |
Katoh, K., Asimenos, G., and Toh, H. (2010). Multiple alignment of DNA sequences with MAFFT. In ‘Bioinformatics for DNA Sequence Analysis’. (Ed. D. Posada.) pp. 39–64. (Human Press: Berlin, Germany.)
Kerbl, A., Bekkouche, N., Sterrer, W., and Worsaae, K. (2015). Detailed reconstruction of the nervous and muscular system of Lobatocerebridae with an evaluation of its annelid affinity. BMC Evolutionary Biology 15, 277.
| Detailed reconstruction of the nervous and muscular system of Lobatocerebridae with an evaluation of its annelid affinity.Crossref | GoogleScholarGoogle Scholar |
Kerbl, A., Fofanova, E. G., Mayorova, T. D., Voronezhskaya, E. E., and Worsaae, K. (2016). Comparison of neuromuscular development in two dinophilid species (Annelida) suggests progenetic origin of Dinophilus gyrociliatus. Frontiers in Zoology 13, 49.
| Comparison of neuromuscular development in two dinophilid species (Annelida) suggests progenetic origin of Dinophilus gyrociliatus.Crossref | GoogleScholarGoogle Scholar |
Kristensen, M. R., and Nørrevang, A. (1982). Description of Psammodrilus aedificator sp. n. (Polychaeta), with notes on the Arctic interstitial fauna of Disko Island, W. Greenland. Zoologica Scripta 11, 265–279.
| Description of Psammodrilus aedificator sp. n. (Polychaeta), with notes on the Arctic interstitial fauna of Disko Island, W. Greenland.Crossref | GoogleScholarGoogle Scholar |
Kvist, S., and Siddall, M. E. (2013). Phylogenomics of Annelida revisited: a cladistic approach using genome-wide expressed sequence tag data mining and examining the effects of missing data. Cladistics 29, 435–448.
| Phylogenomics of Annelida revisited: a cladistic approach using genome-wide expressed sequence tag data mining and examining the effects of missing data.Crossref | GoogleScholarGoogle Scholar |
Laumer, C. E., Bekkouche, N., Kerbl, A., Goetz, F., Neves, R. C., Sørensen, M. V., Kristensen, R. M., Hejnol, A., Dunn, C. W., Giribet, G., and Worsaae, K. (2015). Spiralian phylogeny informs the evolution of microscopic lineages. Current Biology 25, 2000–2006.
| Spiralian phylogeny informs the evolution of microscopic lineages.Crossref | GoogleScholarGoogle Scholar |
Lee, D.-C., and Bryant, H. N. (1999). A reconsideration of the coding of inapplicable characters: assumptions and problems. Cladistics 15, 373–378.
| A reconsideration of the coding of inapplicable characters: assumptions and problems.Crossref | GoogleScholarGoogle Scholar |
Lewis, P. O. (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50, 913–925.
| A likelihood approach to estimating phylogeny from discrete morphological character data.Crossref | GoogleScholarGoogle Scholar |
Maddison, D. R., and Maddison, W. P. (2001). ‘MacClade 4.’ (Sinauer Associates: Sunderland, UK.)
Maddison, W. P., and Maddison, D. R. (2007). Mesquite: a modular system for evolutionary biology. Version 2.0. Available at http:\\mesquiteproject.org [verified 13 June 2018]
Martínez, A., Di Domenico, M., Jörger, K., Norenburg, J., and Worsaae, K. (2013). Description of three new species of Protodrilus (Annelida, Protodrilidae) from Central America. Marine Biology Research 9, 676–691.
| Description of three new species of Protodrilus (Annelida, Protodrilidae) from Central America.Crossref | GoogleScholarGoogle Scholar |
Martínez, A., Di Domenico, M., Rouse, G., and Worsaae, K. (2015). Phylogeny of Protodrilidae (Annelida) inferred by total evidence analyses. Cladistics 31, 250–276.
| Phylogeny of Protodrilidae (Annelida) inferred by total evidence analyses.Crossref | GoogleScholarGoogle Scholar |
Mastepanova, E. A. (2004). The interstitial Polychaeta of Russian seas. Invertebrate Zoology 1, 59–64.
Meyer, R., and Bartolomaeus, T. (1997). Ultrastruktur und Morphogenese der Hakenborsten bei Psammodrilus balanoglossoides – Bedeutung für die Stellung der Psammodrilus (Annelida). Microfauna Marina 11, 87–113.
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, Lousiana, 1–8’.
Parry, L. A., Edgecombe, G. D., Eibye-Jacobsen, D., and Vinther, J. (2016). The impact of fossil data on annelid phylogeny inferred from discrete morphological characters. Proceedings of The Royal Society Series B 283, 20161378.
| The impact of fossil data on annelid phylogeny inferred from discrete morphological characters.Crossref | GoogleScholarGoogle Scholar |
Pleijel, F. (1995). On character coding for phylogeny reconstruction. Cladistics 11, 309–315.
| On character coding for phylogeny reconstruction.Crossref | GoogleScholarGoogle Scholar |
Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., Sundberg, P., and Thollesson, M. (2008). Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.
| Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies.Crossref | GoogleScholarGoogle Scholar |
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., and Drummond, A. J. (2007). Tracer v1.4. Available at http://tree.bio.ed.ac.uk/software/tracer/.
Rieger, R. M. (1980). A new group of interstitial worms, Lobatocerebridae nov. fam. (Annelida) and its significance for metazoan phylogeny. Zoomorphologie 95, 41–84.
| A new group of interstitial worms, Lobatocerebridae nov. fam. (Annelida) and its significance for metazoan phylogeny.Crossref | GoogleScholarGoogle Scholar |
Riser, N. W. (1984). General observations on the intertidal interstitial fauna of New Zealand. Tane 30, 239–250.
Rouse, G. W., and Pleijel, F. (2001). ‘Polychaetes.’ (Oxford University Press: Oxford, UK.)
Salvini-Plawen, L. (1968). Zur Kenntnis des Mesopsammales der Nord Adria I: die für den Meeresteil neuen Gruppen und Arten. Thalassia Jugoslavica 4, 11–17.
Sánchez, N., Yamasaki, H., Pardos, F., Sørensen, M. V., and Martínez, A. (2016). Morphology disentangles the systematics of a ubiquitous but elusive meiofaunal group (Kinorhyncha: Pycnophyidae). Cladistics 32, 479–505.
| Morphology disentangles the systematics of a ubiquitous but elusive meiofaunal group (Kinorhyncha: Pycnophyidae).Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar |
Stocsits, R., Letsch, H., Hertel, J., Misof, B., and Stadler, P. (2009). Accurate and efficient reconstruction of deep phylogenies from structured RNAs. Nucleic Acids Research 37, 6184–6193.
| Accurate and efficient reconstruction of deep phylogenies from structured RNAs.Crossref | GoogleScholarGoogle Scholar |
Strong, E. E., and Lipscomb, D. (1999). Character coding and inapplicable data. Cladistics 15, 363–371.
| Character coding and inapplicable data.Crossref | GoogleScholarGoogle Scholar |
Struck, T. H., Paul, C., Hill, N., Hartmann, S., Hosel, C., Kube, M., Lieb, B., Meyer, A., Tiedemann, R., Purschke, G., and Bleidorn, C. (2011). Phylogenomic analyses unravel annelid evolution. Nature 471, 95–98.
| Phylogenomic analyses unravel annelid evolution.Crossref | GoogleScholarGoogle Scholar |
Struck, T. H., Golombek, A., Weigert, A., Franke, F. A., Westheide, W., Purschke, G., Bleidorn, C., and Halanych, K. M. (2015). The evolution of annelids reveals two adaptive routes to the interstitial realm. Current Biology 25, 1993–1999.
| The evolution of annelids reveals two adaptive routes to the interstitial realm.Crossref | GoogleScholarGoogle Scholar |
Swedmark, B. (1952). Note préliminaire sur un polychète sédentaire aberrant, Psammodrilus balanoglossoides n. g. n. sp. Arkiv för Zoologi 4, 159–162.
Swedmark, B. (1954). Etude du développement larvaire et remarques sur la morphologie de Protodrilus symbioticus Giard (Archiannélides). Arkiv för Zoologi 6, 511–522.
Swedmark, B. (1955). Recherches sur la morphologie le developpement et la biologie de Psammodrilus balanoglossoides, polychète sedentaire de la microfaune des sables. Archive de Zoologie Expérimentale Générale 92, 141–220.
Swedmark, B. (1958). Psammodriloides fauveli n. gen. n. sp. et la famille des Psammodrilidae (Polychaeta Sedentaria). Arkiv för Zoologi, sér 2, 55–65.
Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). ClustalW: 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.
| ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar |
Tzetlin, A. B., and Saphonov, M. V. (2002). Interstitial polychaetes (Annelida) from the Kandalaksha Bay of the White Sea. Зоологический журнал 81, 899–908.
Tzetlin, A. B., Purschke, G., Westheide, W., and Saphonov, M. V. (1992). Ultrastructure of enteronephridia and general description of the alimentary canal in Trochonerilla mobilis and Nerillidium troglochaetoides (Polychaeta, Nerillidae). Acta Zoologica 73, 163–176.
| Ultrastructure of enteronephridia and general description of the alimentary canal in Trochonerilla mobilis and Nerillidium troglochaetoides (Polychaeta, Nerillidae).Crossref | GoogleScholarGoogle Scholar |
Vaidya, G., Lohman, D. J., and Meier, R. (2011). SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171–180.
| SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information.Crossref | GoogleScholarGoogle Scholar |
Varón, A., Vinh, L. S., and Wheeler, W. C. (2010). POY version 4: phylogenetic analysis using dynamic homologies. Cladistics 26, 72–85.
| POY version 4: phylogenetic analysis using dynamic homologies.Crossref | GoogleScholarGoogle Scholar |
Weigert, A., and Bleidorn, C. (2016). Current status of annelid phylogeny. Organisms, Diversity & Evolution 16, 345–362.
| Current status of annelid phylogeny.Crossref | GoogleScholarGoogle Scholar |
Weigert, A., Helm, C., Meyer, M., Nickel, B., Arendt, D., Hausdorf, B., Santos, S. R., Halanych, K. M., Purschke, G., and Bleidorn, C. (2014). Illuminating the base of the annelid tree using transcriptomics. Molecular Biology and Evolution 31, 1391–1401.
| Illuminating the base of the annelid tree using transcriptomics.Crossref | GoogleScholarGoogle Scholar |
Westheide, W. (1982). Ikosipodus carolensis gen. et sp. n., an interstitial neotenic polychaete from North Carolina, USA, and its phylogenetic relationships within Dorvilleidae. Zoologica Scripta 11, 117–126.
| Ikosipodus carolensis gen. et sp. n., an interstitial neotenic polychaete from North Carolina, USA, and its phylogenetic relationships within Dorvilleidae.Crossref | GoogleScholarGoogle Scholar |
Westheide, W. (1987). Progenesis as a principle in meiofauna evolution. Journal of Natural History 21, 843–854.
| Progenesis as a principle in meiofauna evolution.Crossref | GoogleScholarGoogle Scholar |
Westheide, W. (2008). Polychaetes: interstitial families: keys and notes for the identification of the species. Synopsis of the British fauna (New Series), 44 (second edition), 177pp. (Field Studies Council: Shrewsbury, UK)
Westheide, W., and Riser, N. W. (1983). Morphology and phylogenetic relationships of the neotenic interstitial polychaete Apodotrocha progenerans n. gen. n. sp. (Annelida). Zoomorphology 103, 67–87.
| Morphology and phylogenetic relationships of the neotenic interstitial polychaete Apodotrocha progenerans n. gen. n. sp. (Annelida).Crossref | GoogleScholarGoogle Scholar |
Wheeler, W. (1996). Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12, 1–9.
| Optimization alignment: the end of multiple sequence alignment in phylogenetics?Crossref | GoogleScholarGoogle Scholar |
Wheeler, W., Aagesen, L., Arango, C. P., Faivovich, J., Grant, T., D’Haese, C., Janies, D., Smith, W. L., Varón, A., and Giribet, G. (2006). ‘Dynamic Homology and Phylogenetic Systematics: a Unified Approach Using POY.’ (The American Museum of Natural History: New York, NY.)
Wiens, J. J. (2001). Character analysis in morphological phylogenetics: problems and solutions. Systematic Biology 50, 689–699.
| Character analysis in morphological phylogenetics: problems and solutions.Crossref | GoogleScholarGoogle Scholar |
Worsaae, K. (2005a). Phylogeny of Nerillidae (Polychaeta, Annelida) as inferred from combined 18S rDNA and morphological data. Cladistics 21, 143–162.
| Phylogeny of Nerillidae (Polychaeta, Annelida) as inferred from combined 18S rDNA and morphological data.Crossref | GoogleScholarGoogle Scholar |
Worsaae, K. (2005b). Systematics of Nerillidae (Polychaeta, Annelida). Meiofauna Marina 14, 49–74.
Worsaae, K., and Kristensen, R. M. (2005). Evolution of interstitial Polychaeta (Annelida). Hydrobiologia 535-536, 319–340.
| Evolution of interstitial Polychaeta (Annelida).Crossref | GoogleScholarGoogle Scholar |
Worsaae, K., and Sterrer, W. (2006). Description of two new interstitial species of Psammodrilidae (Annelida) from Bermuda. Marine Biology Research 2, 431–445.
| Description of two new interstitial species of Psammodrilidae (Annelida) from Bermuda.Crossref | GoogleScholarGoogle Scholar |
Worsaae, K., Kvindebjerg, K., and Martínez, A. (2015). Morphology of a new interstitial Psammodrilus (Psammodrilidae, Annelida) from Sardinia, Italy. Zoologischer Anzeiger 259, 13–21.
| Morphology of a new interstitial Psammodrilus (Psammodrilidae, Annelida) from Sardinia, Italy.Crossref | GoogleScholarGoogle Scholar |
Xia, X., and Lemey, P. (2009). Assessing substitution saturation with DAMBE. In ‘The Phylogenetic Handbook’. (Eds P. Lemey, M. Salemi, A. M. Vandamme.) pp. 611–626. (Cambridge University Press: Cambridge, UK.)
Yamasaki, H., Hiruta, S. F., and Kajihara, H. (2013). Molecular phylogeny of kinorhynchs. Molecular Phylogenetics and Evolution 67, 303–310.
| Molecular phylogeny of kinorhynchs.Crossref | GoogleScholarGoogle Scholar |
Zanol, J., Fauchald, C., and Paiva, P. C. (2007). A phylogenetic analysis of the genus Eunice (Eunicidae, Polychaeta, Annelida). Zoological Journal of the Linnean Society 150, 413–434.
| A phylogenetic analysis of the genus Eunice (Eunicidae, Polychaeta, Annelida).Crossref | GoogleScholarGoogle Scholar |