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Through the magnifying glass - The big small world of marine meiofauna: Morphology, species and evolution in Nemertodermatida
Stockholm University, Faculty of Science, Department of Zoology. Naturhistoriska riksmuseet, Enheten för zoologi; Swedish Museum of Natural History, Department of Zoology.ORCID iD: 0000-0001-8809-6753
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Nemertodermatida is a group of microscopic marine worm-like animals that live as part of the marine meiofauna in sandy or muddy sediments; one species lives commensally in a holothurian. These benthic worms were thought to disperse passively with ocean currents, resulting in little speciation and thus wide or even cosmopolitan distributions. Individuals occur in low abundance and have few light microscopically available characters, which altogether may explain why only eight species had been described between the discovery of the taxon in 1930 and this thesis. We used molecular methods to address the diversity and phylogeny of this group for the first time. In a study of two nominal species with samples from all around the world, a high degree of cryptic speciation was discovered and several new species described. Diagnoses were based on molecular data complemented by morphological characters, where available. Given the patchy geographical record it can be assumed that the majority of the biodiversity of Nemertodermatida is yet to be described. A phylogenetic study including all but three known species revealed a deep divergence between the two families of Nemertodermatida but non-monophyly of the taxon was rejected by an Approximately Unbiased test.

Confocal laser scanning microscopic studies of several species show that the pattern of the body-wall musculature and the nervous system are specific for different genera. The muscular system of all species consists of a basic orthogonal grid with specific diagonal musculature and specialized muscles associated with body openings. The mouth appears to be transient feature in Nemertodermatida, developing only after hatching and being reduced again in mature worms. The nervous system is highly variable with very different ground patterns between the genera, such as an epidermal net, a centralized neuropile or a commissural brain.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2014. , 41 p.
Keyword [en]
Nemertodermatida, Acoelomorpha, morphology, CLSM, Phalloidin, musculature, DNA, cryptic species, species delimitation, dispersal, taxonomy, phylogenetics, IHC, nervous system
National Category
Biological Systematics Zoology
Research subject
Systematic Zoology
Identifiers
URN: urn:nbn:se:su:diva-107590ISBN: 978-91-7447-986-7 (print)OAI: oai:DiVA.org:su-107590DiVA: diva2:748765
Public defence
2014-10-24, Stora Hörsalen, Naturhistoriska riksmuseet, Frescativägen 40, Stockholm, 13:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council, 2012-3913
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4. Manuscript.

Available from: 2014-10-02 Created: 2014-09-22 Last updated: 2014-11-18Bibliographically approved
List of papers
1. The muscular system of Nemertoderma westbladi and Meara stichopi (Nemertodermatida, Acoelomorpha)
Open this publication in new window or tab >>The muscular system of Nemertoderma westbladi and Meara stichopi (Nemertodermatida, Acoelomorpha)
2013 (English)In: Zoomorphology, ISSN 0720-213X, E-ISSN 1432-234X, Vol. 132, no 3, 239-252 p.Article in journal (Refereed) Published
Abstract [en]

Nemertodermatida is a small taxon of marine worm-like animals; its position in the tree of life is highly contested The musculature of Nemertoderma westbladi and Meara stichopi is studied here in detail using fluorescent phalloidin and confocal microscopy.

In both species the musculature is composed of an outer layer of circular and an inner layer of longitudinal musculature, diagonal muscles form a distinct layer in N westbladi but in M. stichopi these fibres connect to both other layers. The supraterminally opening male pore and antrum are formed by invagination of the whole body-wall in both species and the seminal vesicle is lined by a thin net of musculature only in full male maturity. Modifications of the ventral body-wall adjacent to the mouth are small and transient in N. westbladi including no extra musculature whereas it consists of additional strong U-shaped musculature in M. stichopi. Myogenesis in N. westbladi is not finished in hatchlings and will be completed dorsally in juvenile specimens and ventrally in male mature ones, after the loss of the mouth.

Musculature between the two species differs considerably and might give insights into the internal relationships of Nemertodermatida and might prove to be useful in studies investigating their phylogenetic position. More data of other species and developmental changes are needed.

Place, publisher, year, edition, pages
New York/Heidelberg: Springer, 2013
Keyword
Nemertodermatida, Acoelomorpha, Musculature, Myogenesis, Phalloidin
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-89583 (URN)10.1007/s00435-013-0191-6 (DOI)
Available from: 2013-04-29 Created: 2013-04-29 Last updated: 2017-12-06Bibliographically approved
2. Hyper-Cryptic Marine Meiofauna: Species Complexes in Nemertodermatida
Open this publication in new window or tab >>Hyper-Cryptic Marine Meiofauna: Species Complexes in Nemertodermatida
2014 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 9, e107688Article in journal (Refereed) Published
Abstract [en]

Nemertodermatida are microscopically small, benthic marine worms. Specimens of two nominal species, Sterreria psammicola and Nemertinoides elongatus from 33 locations worldwide were sequenced for three molecular markers. Species delimitation and validation was done using gene trees, haplotype networks and multilocus Bayesian analysis. We found 20 supported species of which nine: Nemertinoides glandulosum n.sp., N. wolfgangi n.sp., Sterreria boucheti n.sp., S. lundini n.sp., S. martindalei n.sp., S. monolithes n.sp., S. papuensis n.sp., S. variabilis n.sp. and S. ylvae n.sp., are described including nucleotide-based diagnoses. The distribution patterns indicate transoceanic dispersal in some of the species. Sympatric species were found in many cases. The high level of cryptic diversity in this meiofauna group implies that marine diversity may be higher than previously estimated. 

Keyword
Nemertodermatida, marine meiofauna, marine biodiversity, cryptic species, species delimitation
National Category
Biological Systematics Zoology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-107585 (URN)10.1371/journal.pone.0107688 (DOI)000344317700074 ()
Funder
Swedish Research Council, 2012-3913
Available from: 2014-09-22 Created: 2014-09-22 Last updated: 2017-12-05Bibliographically approved
3. A multigene molecular assessment reveals deep divergence in the phylogeny of Nemertodermatida
Open this publication in new window or tab >>A multigene molecular assessment reveals deep divergence in the phylogeny of Nemertodermatida
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Here we present a comprehensive phylogeny of Nemertodermatida, a taxon of microscopic marine worms, based for the first on molecular marker with consideration of morphological characters. Our dataset comprises three nuclear genes and most nominal and putative species including recently described cryptic species; only species of the genus Ascoparia could not be obtained. We show that the two families of Nemertodermatida, Ascopariidae and Nemertodermatidae, are retrieved as separate clusters, although not in all analyses as sister groups. We also validate sequences published before 2013 against our dataset; some sequences are shown to be chimeric and have falsified prior hypotheses about nemertodermatid phylogeny, other sequences should be assigned new names. We also show that the genus Nemertoderma needs revision. 

Keyword
Nemertodermatida, LSU, SSU, molecular phylogeny, cryptic species, Approximately Unbiased test
National Category
Zoology Biological Systematics
Research subject
Zoology; Molecular Biology; Systematic Zoology
Identifiers
urn:nbn:se:su:diva-107587 (URN)
Funder
Swedish Research Council, 2012-3913
Available from: 2014-09-22 Created: 2014-09-22 Last updated: 2014-10-28
4. Nervous system and morphology of three species of Nemertodermatida (Acoelomorpha) as revealed by immunostainings, phalloidin staining, confocal and differential contrast microscopy
Open this publication in new window or tab >>Nervous system and morphology of three species of Nemertodermatida (Acoelomorpha) as revealed by immunostainings, phalloidin staining, confocal and differential contrast microscopy
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Nemertodermatida are microscopic marine worms likely to be the sister-group to acoels and the earliest extant bilaterian animals. The nervous system of Flagellophora apelti, Sterreria sp. and Nemertoderma westbladi has been investigated by immunohistochemistry and confocal microscopy using anti-tubulin, anti-5-HT and anti-FMFRamide antibodies as well as by phalloidin staining.

The nervous system of Flagellophora apelti is composed of a large brain neuropile at the level of the statocysts with several fibres surrounding it and innervating the broom organ. Sterreria sp. shows a commissural-like brain and several nerve cords going frontad and caudad from this. At the level of the statocysts there is also a thicker aggregation of IR fibres. The nervous system of N. westbladi consists of a nerve ring lying outside the body wall musculature at the level of the statocyst and a pair of ventro-lateral nerve cords, from which extend numerous fibres innervating the ventral side of the animal. Numerous bottle-shaped glands were observed, innervated by fibres starting both from the brain and the cords. Those nemertodermatids studied to-date display no common nervous system pattern. This study demonstrates that the nemertodermatid nervous system possesses a number of plesiomorphic features and appears more primitive than the nervous system in other worms, except Xenoturbellida. The musculature of Sterreria sp., as revealed by phalloidin-TRITC staining, shows diagonal muscles in the anterior quarter of the body and a simple orthogonal grid in the posterior three quarters. It is more primitive than that of the other nemertodermatids. High-resolution differential contrast microscopy permitted to better visualise some morphological characters such as statocysts, sperm and glands. 

Keyword
Flagellophora apelti, Sterreria sp., Nemertoderma westbladi, Nemertodermatida, nervous system, immunocytochemistry, musculature, statocyst, broom organ, bottle-shaped glands, sperm
National Category
Zoology Biological Systematics
Research subject
Zoology; Molecular Biology; Systematic Zoology
Identifiers
urn:nbn:se:su:diva-107588 (URN)
Funder
Swedish Research Council, 2012-3913
Available from: 2014-09-22 Created: 2014-09-22 Last updated: 2014-10-28

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