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Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Species delimitation integrative approach reveals three new species in the Nemertopsis bivittata complex

Cecili B. Mendes https://orcid.org/0000-0002-9041-1270 A C , Jon L. Norenburg B and Sónia C. S. Andrade https://orcid.org/0000-0002-1302-5261 A C
+ Author Affiliations
- Author Affiliations

A Laboratório de Diversidade Genômica, Departamento de Genética e Biologia Evolutiva, IB (USP), 277 Matao Street, São Paulo, SP, Brazil.

B National Museum of Natural History, Smithsonian Institution, 10th Street & Constitution Avenue NW, Washington, DC 20560, USA.

C Corresponding authors. Email: cecilimendes@ib.usp.br; soniacsandrade@ib.usp.br

Invertebrate Systematics 35(6) 637-654 https://doi.org/10.1071/IS20048
Submitted: 14 June 2020  Accepted: 19 January 2021   Published: 13 August 2021

Abstract

The presence of cryptic species is fairly frequent in many invertebrate groups and even more so among invertebrates with simple morphology, such as nemerteans. Consequently, the use of molecular methods for species delimitation has become a needed tool to complement morphological analyses to better recognise such species. Nemertopsis bivittata is one example of species with subtle morphological variation, but ample geographic distribution, being a good candidate for a species complex study. Here we applied two mitochondrial genes, and 2903 single nucleotide polymorphism (SNP) variants in addition to morphological characters to investigate the presence of cryptic species among specimens previously identified as N. bivittata along the Brazilian Coast. To do so, specimens were collected at 15 different sites in the north-east, south-east and southern regions. Three new species of Nemertopsis are described based on morphological and molecular analyses: Nemertopsis caete sp. nov., Nemertopsis pamelaroeae sp. nov. and Nemertopsis berthalutzae sp. nov. The species N. pamelaroeae and N. berthalutzae present broad distributions from north-east to south-east; N. caete, however, is restricted to the north-east coast. This is the first study to use this combined approach in nemerteans and shows the advantages of integrating genomic markers with classical taxonomy, and applying objective approaches to delimiting species as independently evolving entities.

Keywords: biodiversity, genetics, mitochondrial DNA, molecular taxonomy, Nemertea, South America, species delineation, taxonomy


References

Abadi, S., Azouri, D., Pupko, T., and Mayrose, I. (2019). Model selection may not be a mandatory step for phylogeny reconstruction. Nature Communications 10, 934.
Model selection may not be a mandatory step for phylogeny reconstruction.Crossref | GoogleScholarGoogle Scholar | 30804347PubMed |

Adams, M., Raadik, T. A., Burridge, C. P., and Georges, A. (2014). Global biodiversity assessment and hyper-cryptic species complexes: more than one species of elephant in the room? Systematic Biology 63, 518–533.
Global biodiversity assessment and hyper-cryptic species complexes: more than one species of elephant in the room?Crossref | GoogleScholarGoogle Scholar | 24627185PubMed |

Andrade, S. C. S., Norenburg, J. L., and Solferini, V. N. (2011). Worms without borders: genetic diversity patterns in four Brazilian Ototyphlonemertes species (Nemertea, Hoplonemertea). Marine Biology 158, 2109–2124.
Worms without borders: genetic diversity patterns in four Brazilian Ototyphlonemertes species (Nemertea, Hoplonemertea).Crossref | GoogleScholarGoogle Scholar |

Asch, R. G., Cheung, W. W. L., and Reygondeau, G. (2018). Future marine ecosystem drivers, biodiversity, and fisheries maximum catch potential in Pacific Island countries and territories under climate change. Marine Policy 88, 285–294.
Future marine ecosystem drivers, biodiversity, and fisheries maximum catch potential in Pacific Island countries and territories under climate change.Crossref | GoogleScholarGoogle Scholar |

Bailey, S. A. (2015). An overview of thirty years of research on ballast water as a vector for aquatic invasive species to freshwater and marine environments. Aquatic Ecosystem Health & Management 18, 261–268.
An overview of thirty years of research on ballast water as a vector for aquatic invasive species to freshwater and marine environments.Crossref | GoogleScholarGoogle Scholar |

Bocek, M., Motyka, M., Kusy, D., and Bocak, L. (2019). Genomic and mitochondrial data identify different species boundaries in aposematically polymorphic Eniclases net-winged beetles (Coleoptera: Lycidae). Insects 10, 295.
Genomic and mitochondrial data identify different species boundaries in aposematically polymorphic Eniclases net-winged beetles (Coleoptera: Lycidae).Crossref | GoogleScholarGoogle Scholar |

Bray, T. C., and Bocak, L. (2016). Slowly dispersing neotenic beetles can speciate on a penny coin and generate space-limited diversity in the tropical mountains. Scientific Reports 6, 33579.
Slowly dispersing neotenic beetles can speciate on a penny coin and generate space-limited diversity in the tropical mountains.Crossref | GoogleScholarGoogle Scholar | 27633844PubMed |

Bürger, O. (1895). ‘Die Nemertinen des Golfes von Neapel und der angrenzenden Meeres-Abschnitte.’ (Verlag von R. Friedländer & Sohn.)

Campbell, E. O., Gage, E. V., Gage, R. V., and Sperling, F. A. H. (2020). Single nucleotide polymorphism-based species phylogeny of greater fritillary butterflies (Lepidoptera: Nymphalidae: Speyeria) demonstrates widespread mitonuclear discordance. Systematic Entomology 45, 269–280.
Single nucleotide polymorphism-based species phylogeny of greater fritillary butterflies (Lepidoptera: Nymphalidae: Speyeria) demonstrates widespread mitonuclear discordance.Crossref | GoogleScholarGoogle Scholar |

Caplins, S., Norenburg, J. L., and Turbeville, J. M. (2012). Molecular and morphological variation in the barnacle predator Nemertopsis bivitatta [sic] (Nemertea, Hoplonemertea). Integrative and Comparative Biology 52, E24.

Carlton, J. T. (1985). Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanography and Marine Biology 23, 313–371.

Cherneva, I. A., Chernyshev, A. V., Ekimova, I. A., Polyakova, N. E., Schepetov, D. M., Turanov, S. V., Neretina, T. V., Chaban, E. M., and Malakhov, V. V. (2019). Species identity and genetic structure of nemerteans of the ‘Lineus ruberviridis’ complex (Muller, 1774) from Arctic waters. Polar Biology 42, 497–506.
Species identity and genetic structure of nemerteans of the ‘Lineus ruberviridis’ complex (Muller, 1774) from Arctic waters.Crossref | GoogleScholarGoogle Scholar |

Coe, W. R. (1905). Nemerteans of the west and northwest coasts of America. Bulletin of the Museum of Comparative Zoology at Harvard College 47, 1–318.

Cornils, A., Wend-Heckmann, B., and Held, C. (2017). Global phylogeography of Oithona similis sl (Crustacea, Copepoda, Oithonidae) – a cosmopolitan plankton species or a complex of cryptic lineages? Molecular Phylogenetics and Evolution 107, 473–485.
Global phylogeography of Oithona similis sl (Crustacea, Copepoda, Oithonidae) – a cosmopolitan plankton species or a complex of cryptic lineages?Crossref | GoogleScholarGoogle Scholar | 28007567PubMed |

Corrêa, D. D. (1955). Os gêneros Emplectonema Stimpson e Nemertopsis Bürger (Hoplonemertini Monostilifera). Boletim da Faculdade de filosofia ciências e letras – Universidade de São Paulo 20, 67–86.
Os gêneros Emplectonema Stimpson e Nemertopsis Bürger (Hoplonemertini Monostilifera).Crossref | GoogleScholarGoogle Scholar |

De Donato, M., Peters, S. O., Mitchell, S. E., Hussain, T., and Imumorin, I. G. (2013). Genotyping-by-sequencing (GBS): a novel, efficient and cost-effective genotyping method for cattle using next-generation sequencing. PLoS One 8, e62137.
Genotyping-by-sequencing (GBS): a novel, efficient and cost-effective genotyping method for cattle using next-generation sequencing.Crossref | GoogleScholarGoogle Scholar | 23690931PubMed |

de Medeiros, B. A. S., and Farrell, B. D. (2018). Whole-genome amplification in double-digest RADseq results in adequate libraries but fewer sequenced loci. PeerJ 6, e5089.
Whole-genome amplification in double-digest RADseq results in adequate libraries but fewer sequenced loci.Crossref | GoogleScholarGoogle Scholar |

Dee, S. G., Torres, M. A., Martindale, R. C., Weiss, A., and DeLong, K. L. (2019). The future of reef ecosystems in the Gulf of Mexico: insights from coupled climate model simulations and ancient hot-house reefs. Frontiers in Marine Science 6, 691.
The future of reef ecosystems in the Gulf of Mexico: insights from coupled climate model simulations and ancient hot-house reefs.Crossref | GoogleScholarGoogle Scholar |

Doyle, J. J., and Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11–15.

Drake, J. M., and Lodge, D. M. (2004). Global hot spots of biological invasions: evaluating options for ballast-water management. Proceedings of the Royal Society of London. Series B, Biological Sciences 271, 575–580.
Global hot spots of biological invasions: evaluating options for ballast-water management.Crossref | GoogleScholarGoogle Scholar |

Dryden, I. L., and Mardia, K. V. (1998). ‘Statistical Shape Analysis.’ (Wiley: Chichester, UK.)

Dupuis, J. R., Roe, A. D., and Sperling, F. A. (2012). Multi‐locus species delimitation in closely related animals and fungi: one marker is not enough. Molecular Ecology 21, 4422–4436.
Multi‐locus species delimitation in closely related animals and fungi: one marker is not enough.Crossref | GoogleScholarGoogle Scholar | 22891635PubMed |

Eaton, D. A. R., and Overcast, I. (2020). Ipyrad: interactive assembly and analysis of RADseq datasets. Bioinformatics 36, 2592–2594.
Ipyrad: interactive assembly and analysis of RADseq datasets.Crossref | GoogleScholarGoogle Scholar |

Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., and Mitchell, S. E. (2011). A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379.
A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species.Crossref | GoogleScholarGoogle Scholar | 21573248PubMed |

Feder, J. L., Xie, X., Rull, J., Velez, S., Forbes, A., Leung, B., Dambroski, H., Filchak, K. E., and Aluja, M. (2005). Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis. Proceedings of the National Academy of Sciences of the United States of America 102, 6573–6580.
Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis.Crossref | GoogleScholarGoogle Scholar | 15851672PubMed |

Fišer, C., Robinson, C. T., and Malard, F. (2018). Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology 27, 613–635.
Cryptic species as a window into the paradigm shift of the species concept.Crossref | GoogleScholarGoogle Scholar | 29334414PubMed |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |

Fowler, A. C. (2015). A simple thousand-year prognosis for oceanic and atmospheric carbon change. Pure and Applied Geophysics 172, 49–56.
A simple thousand-year prognosis for oceanic and atmospheric carbon change.Crossref | GoogleScholarGoogle Scholar |

Gibson, R. (1995). Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution. Journal of Natural History 29, 271–561.
Nemertean genera and species of the world: an annotated checklist of original names and description citations, synonyms, current taxonomic status, habitats and recorded zoogeographic distribution.Crossref | GoogleScholarGoogle Scholar |

Herrera, S., and Shank, T. M. (2016). RAD sequencing enables unprecedented phylogenetic resolution and objective species delimitation in recalcitrant divergent taxa. Molecular Phylogenetics and Evolution 100, 70–79.
RAD sequencing enables unprecedented phylogenetic resolution and objective species delimitation in recalcitrant divergent taxa.Crossref | GoogleScholarGoogle Scholar | 26993764PubMed |

Hiebert, T. C., and Maslakova, S. (2015). Integrative taxonomy of the Micrura alaskensis Coe, 1901 species complex (Nemertea: Heteronemertea), with descriptions of a new genus Maculaura gen. nov. and four new species from the NE Pacific. Zoological Science 32, 615–637.
Integrative taxonomy of the Micrura alaskensis Coe, 1901 species complex (Nemertea: Heteronemertea), with descriptions of a new genus Maculaura gen. nov. and four new species from the NE Pacific.Crossref | GoogleScholarGoogle Scholar | 26654045PubMed |

Junoy, J., Andrade, S. C. S., and Giribet, G. (2010). Phylogenetic placement of a new hoplonemertean species commensal on ascidians. Invertebrate Systematics 24, 616–629.
Phylogenetic placement of a new hoplonemertean species commensal on ascidians.Crossref | GoogleScholarGoogle Scholar |

Katoh, K., Rozewicki, J., and Yamada, K. D. (2019). MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20, 1160–1166.
MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization.Crossref | GoogleScholarGoogle Scholar | 28968734PubMed |

Klingenberg, C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353–357.
MorphoJ: an integrated software package for geometric morphometrics.Crossref | GoogleScholarGoogle Scholar | 21429143PubMed |

Kobayashi, T., and Sota, T. (2019). Divergent host use among cryptic species in the fungivorous ciid beetle Octotemnus laminifrons (Motschulsky, 1860), with descriptions of three new species from Japan. Systematic Entomology 44, 179–191.
Divergent host use among cryptic species in the fungivorous ciid beetle Octotemnus laminifrons (Motschulsky, 1860), with descriptions of three new species from Japan.Crossref | GoogleScholarGoogle Scholar |

Leaché, A. D., Banbury, B. L., Felsenstein, J., De Oca, A. N. M., and Stamatakis, A. (2015). Short tree, long tree, right tree, wrong tree: new acquisition bias corrections for inferring SNP phylogenies. Systematic Biology 64, 1032–1047.
Short tree, long tree, right tree, wrong tree: new acquisition bias corrections for inferring SNP phylogenies.Crossref | GoogleScholarGoogle Scholar | 26227865PubMed |

Leigh, J. W., 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 |

Lewin, H. A., Robinson, G. E., Kress, W. J., Baker, W. J., Coddington, J., Crandall, K. A., Durbin, R., Edwards, S. V., Forest, F., Gilbert, M. T. P., Goldstein, M. M., Grigoriev, I. V., Hackett, K. J., Haussler, D., Jarvis, E. D., Johnson, W. E., Patrinos, A., Richards, S., Castilla-Rubio, J. C., van Sluys, M. A., Soltis, P. S., Xu, X., Yang, H., and Zhang, G. (2018). Earth BioGenome Project: sequencing life for the future of life. Proceedings of the National Academy of Sciences of the United States of America 115, 4325–4333.
Earth BioGenome Project: sequencing life for the future of life.Crossref | GoogleScholarGoogle Scholar | 29686065PubMed |

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 | 12116640PubMed |

Mayr, E. (1947). Ecological factors in speciation. Evolution 1, 263–288.
Ecological factors in speciation.Crossref | GoogleScholarGoogle Scholar |

Mendes, C. B., Norenburg, J. L., Solferini, V. N., and Andrade, S. C. S. (2018). Hidden diversity: phylogeography of genus Ototyphlonemertes Diesing, 1863 (Ototyphlonemertidae: Hoplonemertea) reveals cryptic species and high diversity in Chilean populations. PLoS One 13, e0195833.
Hidden diversity: phylogeography of genus Ototyphlonemertes Diesing, 1863 (Ototyphlonemertidae: Hoplonemertea) reveals cryptic species and high diversity in Chilean populations.Crossref | GoogleScholarGoogle Scholar | 29698411PubMed |

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)’, 14 November 2010, New Orleans, LA, USA’. INSPEC Accession Number 11705685, pp. 1–8. (IEEE.) 10.1109/GCE.2010.5676129

Nguyen, L. T., Schmidt, H. A., von Haeseler, A., and Minh, B. Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.
IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Crossref | GoogleScholarGoogle Scholar | 25371430PubMed |

Norenburg, J. L., Gibson, R., Herrera-Bachiller, A., and Strand, M. (2020). World Nemertea Database. Nemertopsis bivittata (Delle Chiaje, 1841). In ‘World Register of Marine Species’. Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=122715 [Verified 27 May 2020].

Nunes, J. R. S., Liu, S., Pértille, F., Perazza, C. A., Villela, P. M. S., de Almeida-Val, V. M. F., Hilsdorf, A. W. S., Liu, Z., and Coutinho, L. L. (2017). Large-scale SNP discovery and construction of a high-density genetic map of Colossoma macropomum through genotyping-by-sequencing. Scientific Reports 7, 46112.
Large-scale SNP discovery and construction of a high-density genetic map of Colossoma macropomum through genotyping-by-sequencing.Crossref | GoogleScholarGoogle Scholar |

Palumbi, S. R., Martin, A. P., Romano, S., Mcmillan, W., Stice, L., and Grabowski, G. (1991). The simple fools guide to PCR. Special publication, Department of Zoology, University of Hawaii, Honolulu, HI, USA.

Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |

Quattrini, A. M., Wu, T., Soong, K., Jeng, M. S., Benayahu, Y., and McFadden, C. S. (2019). A next generation approach to species delimitation reveals the role of hybridization in a cryptic species complex of corals. BMC Evolutionary Biology 19, 116.
A next generation approach to species delimitation reveals the role of hybridization in a cryptic species complex of corals.Crossref | GoogleScholarGoogle Scholar | 31170912PubMed |

Reyes-Velasco, J., Manthey, J. D., Bourgeois, Y., Freilich, X., and Boissinot, S. (2018). Revisiting the phylogeography, demography and taxonomy of the frog genus Ptychadena in the Ethiopian highlands with the use of genome-wide SNP data. PLoS One 13, e0190440.
Revisiting the phylogeography, demography and taxonomy of the frog genus Ptychadena in the Ethiopian highlands with the use of genome-wide SNP data.Crossref | GoogleScholarGoogle Scholar | 29389966PubMed |

Rohlf, F. J. (2015). The TPS series of software. Hystrix – the Italian Journal of Mammalogy 26, 1–4.

Rosenberg, N. A. (2002). The probability of topological concordance of gene trees and species trees. Theoretical Population Biology 61, 225–247.
The probability of topological concordance of gene trees and species trees.Crossref | GoogleScholarGoogle Scholar | 11969392PubMed |

Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., and Sánchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 3299–3302.
DnaSP 6: DNA sequence polymorphism analysis of large data sets.Crossref | GoogleScholarGoogle Scholar | 29029172PubMed |

Sánchez, M. (1973). Sobre 4 especies de nemertinos de Quintero (Chile). Studies on Neotropical Fauna 8, 195–214.
Sobre 4 especies de nemertinos de Quintero (Chile).Crossref | GoogleScholarGoogle Scholar |

Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology & Evolution 16, 372–380.
Ecology and the origin of species.Crossref | GoogleScholarGoogle Scholar |

Som, A. (2015). Causes, consequences and solutions of phylogenetic incongruence. Briefings in Bioinformatics 16, 536–548.
Causes, consequences and solutions of phylogenetic incongruence.Crossref | GoogleScholarGoogle Scholar | 24872401PubMed |

Sonsthagen, S. A., Wilson, R. E., Chesser, R. T., Pons, J. M., Crochet, P. A., Driskell, A., and Dove, C. (2016). Recurrent hybridization and recent origin obscure phylogenetic relationships within the ‘white-headed’ gull (Larus sp.) complex. Molecular Phylogenetics and Evolution 103, 41–54.
Recurrent hybridization and recent origin obscure phylogenetic relationships within the ‘white-headed’ gull (Larus sp.) complex.Crossref | GoogleScholarGoogle Scholar | 27369453PubMed |

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |

Stec, D., Krzywański, Ł., Zawierucha, K., and Michalczyk, Ł. (2020). Untangling systematics of the Paramacrobiotus areolatus species complex by an integrative redescription of the nominal species for the group, with multilocus phylogeny and species delineation in the genus Paramacrobiotus. Zoological Journal of the Linnean Society 188, 694–716.
Untangling systematics of the Paramacrobiotus areolatus species complex by an integrative redescription of the nominal species for the group, with multilocus phylogeny and species delineation in the genus Paramacrobiotus.Crossref | GoogleScholarGoogle Scholar |

Strand, M., and Sundberg, P. (2011). A DNA-based description of a new nemertean (phylum Nemertea) species. Marine Biology Research 7, 63–70.
A DNA-based description of a new nemertean (phylum Nemertea) species.Crossref | GoogleScholarGoogle Scholar |

Strand, M., Norenburg, J., Alfaya, J. E., Ángel Fernández-Álvarez, F., Andersson, H. S., Andrade, S. C. S., Bartolomaeus, T., Beckers, P., Bigatti, G., Cherneva, I., Chernyshev, A., Chung, B. M., von Döhren, J., Giribet, G., Gonzalez-Cueto, J., Herrera-Bachiller, A., Hiebert, T., Hookabe, N., Junoy, J., Kajihara, H., Krämer, D., Kvist, S., Magarlamov, T. Y., Maslakova, S., Mendes, C. B., Okazaki, R., Sagorny, C., Schwartz, M., Sun, S. C., Sundberg, P., Turbeville, J. M., and Xu, C. M. (2019). Nemertean taxonomy – implementing changes in the higher ranks, dismissing Anopla and Enopla. Zoologica Scripta 48, 118–119.
Nemertean taxonomy – implementing changes in the higher ranks, dismissing Anopla and Enopla.Crossref | GoogleScholarGoogle Scholar |

Strong, E. E., and Whelan, N. V. (2019). Assessing the diversity of western North American Juga (Semisulcospiridae, Gastropoda). Molecular Phylogenetics and Evolution 136, 87–103.
Assessing the diversity of western North American Juga (Semisulcospiridae, Gastropoda).Crossref | GoogleScholarGoogle Scholar | 30974201PubMed |

Sundberg, P., Vodoti, E. T., Zhou, H., and Strand, M. (2009a). Polymorphism hides cryptic species in Oerstedia dorsalis (Nemertea, Hoplonemertea). Biological Journal of the Linnean Society. Linnean Society of London 98, 556–567.
Polymorphism hides cryptic species in Oerstedia dorsalis (Nemertea, Hoplonemertea).Crossref | GoogleScholarGoogle Scholar |

Sundberg, P., Chernyshev, A. V., Kajihara, H., Kånneby, T., and Strand, M. (2009b). Character-matrix based descriptions of two new nemertean (Nemertea) species. Zoological Journal of the Linnean Society 157, 264–294.
Character-matrix based descriptions of two new nemertean (Nemertea) species.Crossref | GoogleScholarGoogle Scholar |

Sundberg, P., Andrade, S. C. S., Bartolomaeus, T., Beckers, P., von Döhren, J., Krämer, D., Gibson, R., Giribet, G., Herrera-Bachiller, A., Junoy, J., Kajihara, H., Kvist, S., Kånneby, T., Sun, S. C., Thiel, M., Turbeville, J. M., and Strand, M. (2016a). The future of nemertean taxonomy (phylum Nemertea) – a proposal. Zoologica Scripta 45, 579–582.
The future of nemertean taxonomy (phylum Nemertea) – a proposal.Crossref | GoogleScholarGoogle Scholar |

Sundberg, P., Kvist, S., and Strand, M. (2016b). Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea). PLoS One 11, e0155541.
Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea).Crossref | GoogleScholarGoogle Scholar | 27171471PubMed |

Toews, D. P. L., and Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21, 3907–3930.
The biogeography of mitochondrial and nuclear discordance in animals.Crossref | GoogleScholarGoogle Scholar |

Zhang, J., Kapli, P., Pavlidis, P., and Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.
A general species delimitation method with applications to phylogenetic placements.Crossref | GoogleScholarGoogle Scholar | 23990417PubMed |

Zhbannikov, I. Y., Hunter, S. S., Foster, J. A., and Settles, M. L. (2017). SeqyClean: a pipeline for high-throughput sequence data preprocessing. In ‘Proceedings of the 8th ACM International Conference on Bioinformatics, Computational Biology, and Health Informatics’, August 2017, Boston, MA, USA. pp. 407–416. (Association for Computing Machinery: New York, NY, USA.)