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Progenetic evolution in the deep-sea fauna

Final Report Summary - PRODEEP (Progenetic evolution in the deep-sea fauna)

The project aimed to achieve understanding of the role of progenesis in colonization of the deep ocean by marine organisms. Hyalinoeciinae, a subfamily of marine bristle worms with cosmopolitan and wide bathymetric distribution has been chosen as an exemplar group to study progenesis in marine invertebrates.
The main objective was to assess the morphological and genetic variation within Hyalinoeciinae. Several large collections of hyalinoeciins from the University Museum of Bergen, Norway; the Natural History Museum in London UK; the Natural History Museum of the Smithsonian Institution, USA; the German Center for Marine Biodiversity Research, Senckenberg Institute, Germany; the Australian Museum; the Shirshov Institute of Oceanology Russian Academy of Sciences, Russia were examined including type and non-type specimens. Morphological study was done using the methods of histology, light, scanning and transmission electron microscopy. Genetic variation was assessed using sequence data of several genes: COI, 16S rDNA, 18S rDNA, 28S rDNA, ITS1, ITS2. Taxonomical revisions of two progenetic genera, Leptoecia and Hyalinoecia, were among the main results of the project. Based on the obtained information, Leptoecia comprised ten species with three species new to science and Hyalinoecia comprised 15 species with two species new to science. A new to science species of Nothra, another hyalinoeciin genus, was described during the project (Budaeva 2015).
The second objective was to assess phylogenetic position of Hyalinoeciinae species with suggested progenetic origin. We reconstructed the first comprehensive phylogeny of the family Onuphidae based on two molecular markers (16S rDNA and 18S rDNA). This reconstruction corroborated previous subdivision of Onuphidae into two monophyletic subfamilies (Hyalinoeciinae and Onuphinae) as well as monophyly of the most accepted genera but did not resolve relationships between the genera within hyalinoeciins (Budaeva et al. 2016). To resolve the phylogeny of Hyalinoeciiae we increased the number of analyzed genetic markers (COI, 16S rDNA, 18S rDNA, 28S rDNA) and included newly sequenced species of Nothia and Anchinothria – non-progenetic genera of the subfamily. The analysis of a complete matrix with no missing sequence data of 18 species resulted in well-supported phylogenetic tree contradicting previously accepted hypotheses on the relationships within Hyalinoeciinae.
The third objective was to trace the evolution of morphological characters within Hyalinoeciinae. We used the reconstructed phylogenetic tree to map morphological characters (presence/absence of peristomial cirri, shape of anterior prechaetal lobes, shape of pectinate chaetae) in order to obtain independent evidences on primary absence or secondary loss of characters in species with presumed progenetic origin. We also studied the ontogeny of several hyalinoeciin species (Leptoecia vivipara, Nothria spp.) to follow the development of selected characters absent or underdeveloped in adult (mature) specimens of progenetic species (Budaeva et al. 2014). Our results show that all studied onuphid worms display similar general pattern of chaetal replacement in ontogeny in combination with successive appearance of prostomial, peristomial and parapodial appendages. Chaetal progression pattern varies between onuphid subfamilies in morphology of provisional juvenile chaetae and order of appearance of the definitive chaetae.
The fourth objective was to develop a hypothesis on the possible pathways of the deep-sea invasion by hyalinoeciins. We focused on two sister genera, so-called quill worms, with organic tubes as they expressed the highest degree of progenesis among hyalinoeciins. Analysis of vertical ranges of species in these genera after complete taxonomical revision revealed a clear break at depth about 2000 m in their distribution with larger and less progenetic Hyalinoecia being mostly present in shallower waters and smaller and juvenile-like Leptoecia widely distributed in the deep sea. The deep-sea Leptoecia species exhibit an extreme mode of parental care being viviparous and carrying developing embryos in the parental body cavity until various advanced stages. Progenesis is a life history strategy, which can be successful in unstable environments with unpredictable fluctuations of scattered, but abundant, resources. We hypothesise that the progenetic appearance and accelerated sexual maturation in deep-sea Leptoecia could have evolved as an adaptation to seasonality of the food supply in the deep-sea high-latitude environment.
The project fully achieved the initial objectives, in particular contributed to the development of systematics, taxonomy and phylogeny of poorly known group of marine bristle worms, understanding of evolution of progenetic deep-sea taxa, and importance of independent assessment of morphological and molecular data. It also improved cooperation between the Norwegian host organization and the Russian community in marine biological research and education strengthening the European scientific expertise and providing future training opportunities.
The project contributed strongly to the transfer of knowledge from the Researcher to the local and international scientific communities via supervision of a MSc student in 2015-2015 working at the University Museum of Bergen on marine annelids, and organization of a 2-week summer school on Systematics, Morphology and Evolution of Annelids at the Espegrend Marine Biological Station of the University of Bergen. The course had 20 participating students from 12 countries and prominent researchers from Europe and USA as contributing instructors.