Patterns of Diversity in Soft-Bodied Meiofauna: Dispersal Ability and Body Size Matter

Background: Biogeographical and macroecological principles are derived from patterns of distribution in large organisms, whereas microscopic ones have often been considered uninteresting, because of their supposed wide distribution. Here, after reporting the results of an intensive faunistic survey of marine microscopic animals (meiofauna) in Northern Sardinia, we test for the effect of body size, dispersal ability, and habitat features on the patterns of distribution of several groups.Methodology/Principal Findings: As a dataset we use the results of a workshop held at La Maddalena (Sardinia, Italy) in September 2010, aimed at studying selected taxa of soft-bodied meiofauna (Acoela, Annelida, Gastrotricha, Nemertodermatida, Platyhelminthes and Rotifera), in conjunction with data on the same taxa obtained during a previous workshop hosted at Tjärnö (Western Sweden) in September 2007. Using linear mixed effects models and model averaging while accounting for sampling bias and potential pseudoreplication, we found evidence that: (1) meiofaunal groups with more restricted distribution are the ones with low dispersal potential; (2) meiofaunal groups with higher probability of finding new species for science are the ones with low dispersal potential; (3) the proportion of the global species pool of each meiofaunal group present in each area at the regional scale is negatively related to body size, and positively related to their occurrence in the endobenthic habitat.Conclusion/Significance: Our macroecological analysis of meiofauna, in the framework of the ubiquity hypothesis for microscopic organisms, indicates that not only body size but mostly dispersal ability and also occurrence in the endobenthic habitat are important correlates of diversity for these understudied animals, with different importance at different spatial scales. Furthermore, since the Western Mediterranean is one of the best-studied areas in the world, the large number of undescribed species (37%) highlights that the census of marine meiofauna is still very far from being complete

Through the magnifying glass - The big small world of marine meiofauna : Morphology, species and evolution in Nemertodermatida

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.At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript.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

Interrelationships of Nemertodermatida

The phylogeny of Nemertodermatida, a group of microscopic marine worms, was analysed using nucleotide sequences from the ribosomal LSU and SSU genes and the protein coding Histone 3 gene. All currently known species except Ascoparia neglecta and A. secunda were included in the study in addition to several yet undescribed species. Ascopariidae and Nemertodermatidae, are retrieved as separate clades, although not in all analyses as sister groups. Non-monophyly of Nemertodermatida was rejected by the Approximately Unbiased test. Nucleotide sequences deposited in Genbank before 2013 as nemertodermatid were validated against our dataset; some of them are shown to be chimeric implying falsification of prior hypotheses about nemertodermatid phylogeny: other sequences should be assigned new names. We also show that the genus Nemertoderma needs revision.

The muscular system of Nemertoderma westbladi and Meara stichopi (Nemertodermatida, Acoelomorpha)

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

Diversity within the genus <i>Sterreria.</i>

<p>a–c: <i>Sterreria lundini</i> n.sp. a) Overview over whole animal. b) Anterior with statocyst with double statoliths and oval frontal gland secretions. c) Posterior with fsv and male pore (mp). d, e: <i>Sterreria psammicola</i>. d) Posterior with fsv male pore (mp) and adhesive area (ad). e) Overview over male mature animal with large epidermal glands distributed more or less evenly over the whole body and mco in the posterior. f) Anterior part of an animal with epidermal glands, statocyst and central frontal gland opening (fp). g–j: <i>Sterreria rubra</i>. g) Posterior with two mature eggs (e) and mco. h) Overview over the same male and female mature specimen with mature eggs (e) and oocytes (oo). i) Anterior with statocyst and rod-shaped frontal gland secretions. j) Detail of the epidermis in the anterior of an animal with cell borders clearly visible, giving the animal a “scaly” appearance. k: <i>Stererria papuensis</i> n.sp. Anterior part of the holotype. All photographs are taken of live specimens in squeeze preparation. a, b, c, f and k are photographs of the holotype and neotype specimens respectively. The scale bars indicate 100 µm for each photograph.</p

Morphological variation within the genera <i>Nemertinoides</i> and <i>Sterreria</i>.

<p>Light microscope photographs of live specimens in squeeze preparation. a) <i>Sterreria rubra</i> from Southern Portugal, b) <i>S. psammicola</i> from Southern Portugal, c) <i>S. martindalei</i> n.sp. from Waimanolo, Hawaii, d) <i>S. ylvae</i> n.sp, from Waimanolo, Hawaii, e) <i>S. variabilis</i> n.sp. from New Caledonia, f) <i>S. variabilis</i> n.sp. from Bermuda, g) <i>Nemertinoides elongatus</i> from Southern Portugal, h) <i>S. rubra</i> from Helgoland, North Sea, i) <i>N. glandulosum</i> n.sp. from Southern Portugal, j) <i>N. wolfgangi</i> n.sp. from Croatia.</p

List of all individuals used in this study sorted by clade, with Zoobank Life Science Identifiers (LSID) where applicable, connecting collection code (used in the scratchpads database for Acoela and Nemertodermatida at http://acoela.myspecies.info/), genbank accession numbers per gene and the museum collection numbers for type material.

<p>N. abbreviates the genus <i>Nemertinoides</i>, S. the genus <i>Sterreria</i>, abbreviations with numbers indicate putative species per genus not formally described in this paper. Type material is deposited at the Swedish Museum of Natural History (SMNH) in Stockholm, Sweden.</p><p>List of all individuals used in this study sorted by clade, with Zoobank Life Science Identifiers (LSID) where applicable, connecting collection code (used in the scratchpads database for Acoela and Nemertodermatida at <a href="http://acoela.myspecies.info/" target="_blank">http://acoela.myspecies.info/</a>), genbank accession numbers per gene and the museum collection numbers for type material.</p

Results of the BP&P analyses for the tested species.

<p>Results given as nodal support for all <i>Nemertinoides</i> species (green in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0107688#pone-0107688-g002" target="_blank">Fig 2</a>), mainly European <i>Sterreria</i> species (red in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0107688#pone-0107688-g002" target="_blank">Fig 2</a>) and the extra-European <i>Sterreria</i> species (blue in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0107688#pone-0107688-g002" target="_blank">Fig 2</a>). Support values are Bayesian posterior probabilities for the different analyses in the order G(1/100), G(1/1000) and old root age (G(1/100) and G(1/10000)). The dataset was split in order to avoid artefacts due to unresolved topologies in the gene trees and increase confidence in the input topologies. Only clades represented by more than two specimens were tested in order to increase confidence.</p

Molecular Diagnostic character of all newly described species in the three genes used in this study.

<p>Numbers refer to positions in the respective alignments and in brackets to the position in the sequences in the type specimen (genbank accession number).</p><p>Molecular Diagnostic character of all newly described species in the three genes used in this study.</p