Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences

Saccocirrids are tiny, slender annelids inhabiting the interstices among coarse sand sediments in shallow waters. The 22 nominal species can be grouped into two morphological groups "papillocercus"and "krusadensis", based on the absence/presence of a pharyngeal bulbus muscle, absence/presence of ventral ciliary patterns, bilateral/unilateral gonad arrangement and chaetal differences. We present herein the first phylogenetic analyses of Saccocirridae based on four molecular markers and 34 morphological characters, employing maximum likelihood and Bayesian methods. All analyses confirmed the monophyly of each morphological group with high nodal support. As a consequence and based on several apomorphic characters, a new genus, Pharyngocirrus gen. nov., is erected for the "krusadensis"clade. Remarkably, the habitat preferences and trophic guilds are also shown to differ between the two genera, yet show strong consistency within each group. Geographic distribution analyses underscore the family preference for subtropical areas, but reject the previously proposed restriction of Pharyngocirrus gen. nov. to the Indo-Pacific. The finding of two morphologically diverging, cosmopolitan sister clades with different habitat preferences suggest an early ecological diversification of the family, conserved during the later evolution, speciation processes and dispersal of the family75202218CONSELHO NACIONAL DE DESENVOLVIMENTO CIENTÍFICO E TECNOLÓGICO - CNPQFUNDAÇÃO DE AMPARO À PESQUISA DO ESTADO DE SÃO PAULO - FAPESP140611/2008-82012/08581-0; 2013/04358-7Det Frie Forskningsrad (DFF); Carlsberg Foundation; Reserva de la Biosfera (Government of Lanzarote

Conservative route to genome compaction in a miniature annelid

The causes and consequences of genome reduction in animals are unclear because our understanding of this process mostly relies on lineages with often exceptionally high rates of evolution. Here, we decode the compact 73.8-megabase genome of Dimorphilus gyrociliatus, a meiobenthic segmented worm. The D. gyrociliatus genome retains traits classically associated with larger and slower-evolving genomes, such as an ordered, intact Hox cluster, a generally conserved developmental toolkit and traces of ancestral bilaterian linkage. Unlike some other animals with small genomes, the analysis of the D. gyrociliatus epigenome revealed canonical features of genome regulation, excluding the presence of operons and trans-splicing. Instead, the gene-dense D. gyrociliatus genome presents a divergent Myc pathway, a key physiological regulator of growth, proliferation and genome stability in animals. Altogether, our results uncover a conservative route to genome compaction in annelids, reminiscent of that observed in the vertebrate Takifugu rubripes

The Potent Respiratory System of Osedax mucofloris (Siboglinidae, Annelida) - A Prerequisite for the Origin of Bone-Eating Osedax?

Members of the conspicuous bone-eating genus, Osedax, are widely distributed on whale falls in the Pacific and Atlantic Oceans. These gutless annelids contain endosymbiotic heterotrophic bacteria in a branching root system embedded in the bones of vertebrates, whereas a trunk and anterior palps extend into the surrounding water. The unique life style within a bone environment is challenged by the high bacterial activity on, and within, the bone matrix possibly causing O2 depletion, and build-up of potentially toxic sulphide. We measured the O2 distribution around embedded Osedax and showed that the bone microenvironment is anoxic. Morphological studies showed that ventilation mechanisms in Osedax are restricted to the anterior palps, which are optimized for high O2 uptake by possessing a large surface area, large surface to volume ratio, and short diffusion distances. The blood vascular system comprises large vessels in the trunk, which facilitate an ample supply of oxygenated blood from the anterior crown to a highly vascularised root structure. Respirometry studies of O. mucofloris showed a high O2 consumption that exceeded the average O2 consumption of a broad line of resting annelids without endosymbionts. We regard this combination of features of the respiratory system of O. mucofloris as an adaptation to their unique nutrition strategy with roots embedded in anoxic bones and elevated O2 demand due to aerobic heterotrophic endosymbionts

Acoelomorpha: earliest branching bilaterians or deuterostomes?

The Acoelomorpha is an animal group comprised by nearly 400 species of misleadingly inconspicuous flatworms. Despite this, acoelomorphs have been at the centre of a heated debate about the origin of bilaterian animals for 150 years. The animal tree of life has undergone major changes during the last decades, thanks largely to the advent of molecular data together with the development of more rigorous phylogenetic methods. There is now a relatively robust backbone of the animal tree of life. However, some crucial nodes remain contentious, especially the node defining the root of Bilateria. Some studies situate Acoelomorpha (and Xenoturbellida) as the sister group of all other bilaterians, while other analyses group them within the deuterostomes which instead suggests that the last common bilaterian ancestor directly gave rise to deuterostomes and protostomes. The resolution of this node will have a profound impact on our understanding of animal/bilaterian evolution. In particular, if acoelomorphs are the sister group to Bilateria, it will point to a simple nature for the first bilaterian. Alternatively, if acoelomorphs are deuterostomes, this will imply that they are the result of secondary simplification. Here, we review the state of this question and provide potential ways to solve this long-standing issue. Specifically, we argue for the benefits of (1) obtaining additional genomic data from acoelomorphs, in particular from taxa with slower evolutionary rates; (2) the development of new tools to analyse the data; and (3) the use of metagenomics or metatranscriptomics data. We believe the combination of these three approaches will provide a definitive answer as to the position of the acoelomorphs in the animal tree of life

Gain Of Palps Within A Lineage Of Ancestrally Burrowing Annelids (scalibregmatidae)

Scalibregmatidae is a small annelid family of subsurface deposit feeders in sand or mud, which are generally well adapted to infaunal burrowing. The overall morphology of Scalibregmatidae is very similar, with thick bodies, small parapodia, and no prostomial appendages or short horns. The only exception is members of the genera Axiokebuita and Speleobregma that most frequently inhabit crevices or gravel and possess extensive ventral ciliated palps and globular adhesive pygidium. Character reconstruction using maximum likelihood and Bayesian methods show that ciliated palps and adhesive pygidium are synapomorphies of the Axiokebuita-Speleobregma clade. The most likely transformation series is from horns to ciliated palps, the origin of which correlates with the occurrence of Axiokebuita and Speleobregma in crevices or gravel. The wide spaces among rocks or granules yield high permeability and inertial water flow, preventing deposition of organic matter. Under these flow conditions that differ significantly from those of sand or mud bottom, ciliated palps aid to the collection of suspended particles and an adhesive pygidium provides attachment. With palps being a highly debated character in annelid evolution, it is remarkable that prominent ciliated palps are gained within a lineage of ancestrally nonpalpate annelids, most likely increasing their fitness when colonizing a new environment. © 2013 The Royal Swedish Academy of Sciences

Phylogeny And Systematics Of Protodrilidae (annelida) Inferred With Total Evidence Analyses

Protodrilidae is a group of small, superficially simple-looking annelids, lacking chaetae and appendages, except for two prostomial palps. Originally considered to be one of the primitive "archiannelid" families, its affinity within Annelida is still highly debated. Protodrilids are found worldwide in the interstices of intertidal and subtidal marine sediments. Despite their simple appearance they constitute one of the most species-rich interstitial families, with 36 described species in two genera, Protodrilus and the gutless Astomus. Here we present the first phylogenetic study of Protodrilidae employing five gene fragments, 55 morphological characters and 73 terminals (including seven outgroups) analysed under direct optimization and parsimony as well as model-based methods. The large data set includes all 36 described species of Protodrilidae (17 of which are represented only by the morphological partition) as well as 30 undescribed or uncertain species (represented by both morphology and molecules). This comprehensive, inclusive and combined analysis revealed a new perspective on the phylogeny of Protodrilidae: the family is shown to contain six cosmopolitan subclades, each supported by several morphological apomorphies, and with the genus Astomus consistently nested among the other five clades rather than next to these. Consequently, the diagnosis of Protodrilus is emended, Astomus remains unchanged and the four remaining lineages are diagnosed and named Megadrilus n. gen, Meiodrilus gen. nov., Claudrilus n. gen and Lindrilus gen. nov. Character transformations showed that large size and presence of pigmentation, oviducts and eyes are plesiomorphies of the family, retained in Protodrilus, Megadrilus gen. nov. and Lindrilus gen. nov. These features are secondarily lost in the gutless Astomus with epidermal uptake of nutrients, as well as in Meiodrilus gen. nov. and some species of Claudrilus n. gen, with smaller size correlated to life in interstices of finer sediments. © The Willi Hennig Society 2014

Evolution of cave Axiokebuita and Speleobregma (Scalibregmatidae, Annelida)

The evolutionary history of Axiokebuita and Speleobregma, two poorly known lineages of annelids exclusive from deep-sea or marine caves but always from crevicular habitats, is explored here. Speleobregma lanzaroteum Bertelsen, 1986, and Axiokebuita cavernicola sp. n. are described from anchialine and marine caves of the Canary Islands using light and electron microscopy. Speleobregma lanzaroteum is previously known only from a single specimen from the water column of an anchialine cave in Lanzarote. Emended diagnosis, details on the ciliary patterns and behavioural observations are provided based on newly collected material and in situ observations. Axiokebuita cavernicola sp. n. is found in Pleistocene gravel deposits in a shallow water marine cave in Tenerife (Canary Islands). The new species is characterized by the presence of dorsal ciliary bands and short knob-like neuropodial cirri from segment two. The porosity and permeability of the gravelly environment of A.cavernicola sp. n. are shown to be equivalent to the water column or crevices of Speleobregma and other Axiokebuita spp. Phylogenetic analyses of five gene fragments and 44 terminals using maximum-likelihood and Bayesian methods support a derived position of A.cavernicola sp. n. within Axiokebuita and confirm a sister-group relationship of Axiokebuita with Speleobregma with high nodal support. The Axiokebuita-Speleobregma clade is morphologically characterized by a globular pygidium with adhesive glands and ventral ungrooved ciliated palps. Our results support two independent cave colonization events, favoured by the preadaptation of the members of Axiokebuita-Speleobregma lineage to crevicular habitats.426623636Uesteyaide Caving Club (Lanzarote)Danish Independent Research Council [272-06-0260]Freja Program, University of CopenhagenCarlsberg Foundation [2010_01_0802]Danish Independent Research Council [272-06-0260]Carlsberg Foundation [2010_01_0802