Evolutionary history, connectivity and habitat-use of annelids from deep-sea chemosynthesis-based ecosystems, with an emphasis on the Arctic mid-Ocean Ridge and the Nordic Seas
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The enigmatic fauna of chemosynthesis-based ecosystems (CBEs), i.e. hydrothermal vents, cold seeps and organic falls, has been the subject of intensive research over the last decades. However, there are still many aspects of these ecosystems that are poorly understood. There are many shared families and genera of animals between the different types of CBEs, which shows that there is an evolutionary link between them, but the prevalence of shared species and present-day connectivity between different CBEs is debated. The existence of “intermediate” habitats such as sedimented hydrothermal vents and hydrothermal seeps, led to the suggestion that CBEs should be considered a continuum of reducing conditions, rather than completely distinct phenomena. However, it is not clear which environmental factors are most important in structuring the fauna of CBEs, or what determines the habitat specificity of taxa. Evolutionary studies of CBE-adapted taxa often show a gradual adaptation to more extreme environments, with organic falls or cold seeps serving as evolutionary stepping-stones into the hydrothermal vent habitat. Most of these studies, however, have been focused on symbiotrophic taxa, and the evolutionary role of intermediate habitats has not been assessed in a phylogenetic context. Sampling of CBEs is still patchy and biased, both in terms of geographic regions and habitats, which hampers our understanding of biogeographic patterns. The main objective of this project was to contribute to filling these knowledge gaps by focusing on the annelid fauna of CBEs on the Arctic Mid-Ocean Ridge and in the Nordic Seas. The target taxa were worms in the family Ampharetidae, which are commonly found in all types of CBEs around the world, and Sclerolinum contortum and Nicomache lokii, which are abundant habitat-builders in Arctic CBEs. The project aimed to: 1 – describe the new species of Ampharetidae from Loki’s Castle Vent Field (LCVF), 2 – reconstruct the evolutionary history of Ampharetidae, 3 – assess the relationship between the Arctic populations of Sclerolinum contortum and Nicomache lokii, and populations in other oceans, 4 – reassess the links between the annelid fauna of Loki’s Castle Vent Field and vent faunas of other oceans, and 5 – evaluate which environmental factors may be driving the habitat-specificity and distributions of the studied species. The new species of Ampharetidae from Loki’s Castle were formally described as Pavelius smileyi sp. nov. and Paramytha schanderi gen. et sp. nov. Phylogenetic reconstructions and inference of ancestral habitats revealed that adaptation to CBEs has happened multiple times independently within Ampharetidae. Multiple independent colonisations of CBEs within a family is unusual, but may be more common in heterotrophic taxa. The habitat transitions recovered were both from seep to vent and vent to seep, which contradicts the notion of gradual adaptation into more and more extreme habitats, with hydrothermal vents considered the most extreme. Sedimented vents were involved in two of the three transitions inferred, which supports the hypothesis that sedimented vents are important in linking vents and seeps, and a novel link between organic falls and sedimented vents was also shown in a clade comprising the genera Paramytha and Decemunciger. Both Sclerolinum contortum and Nicomache lokii were shown to be distributed all the way from the Arctic to the Antarctic, which is the widest geographic range of animals from CBEs known to date. This corroborates findings by other authors indicating that wide geographic ranges might not be unusual for annelids from CBEs. S. contortum shows a stronger geographic structure in the haplotype networks than N. lokii, but whether this is due to different dispersal capacities or reflects the geographic isolation of the sampled localities is unclear. Two distinct mitochondrial lineages of N. lokii are present in the Antarctic, which may be the result of two independent colonization events. The wide ranges observed in these species may be facilitated by their ability to colonize different types of CBEs, and it is likely that population connectivity is maintained through presently unknown populations. The presence of taxa at LCVF belonging to genera common at Pacific vents such as Amphisamytha and Nicomache, led to the hypothesis that the fauna at LCVF was partly formed by migrations from the Pacific. However, the results presented here show that ampharetid species from LCVF belong to globally distributed clades and have no clear geographic affinities. In addition, the wide distributions of Sclerolinum contortum and Nicomache lokii indicate a higher degree of connectivity between Arctic and Atlantic CBEs than previously recognized. Although most ampharetids are specific to one type of CBE, a review of the habitatuse of ampharetid species showed that they are quite flexible in terms of substratum, temperature and fluid flux. Depth and biological interactions may play a role in determining the habitat specificity and distributions of ampharetids, but we will probably find more examples of ampharetids inhabiting multiple CBEs in the future. Observations on the environmental conditions inhabited by Sclerolinum contortum and Nicomache lokii indicates that S. contortum may be able to occupy areas of lower sulphide levels, but is limited by high temperatures. On the other hand, N. lokii seems to be more temperature tolerant, but may require higher levels of sulphide. These findings support the notion that environmental factors varying across habitats, such as fluid flux, are important in shaping the faunal composition of CBEs. The results presented in this thesis shows that there is still a lot of undescribed biodiversity in CBEs, and illustrates the need for integrative taxonomic work. The importance of comparing across habitats and geographic regions is also demonstrated, and future collaborative projects will hopefully enable a better understanding of large scale patterns and the underlying processes in CBEs.
Has partsPaper I: Kongsrud, J.A., Eilertsen, M.H., Alvestad, T., Kongshavn, K. & Rapp, H.T. (2017) New species of Ampharetidae (Annelida: Polychaeta) from the Arctic Loki Castle vent field. Deep Sea Research Part II Topical Studies in Oceanography, 137: 232-245. The article is available at: http://hdl.handle.net/1956/16250
Paper II: Eilertsen, M.H., Kongsrud, J.A., Alvestad, T., Stiller, J., Rouse, G.W., Rapp, H.T. (2017) Do ampharetids take sedimented steps between vents and seeps? Phylogeny and habitat-use of Ampharetidae (Annelida, Terebelliformia) in chemosynthesis-based ecosystems. BMC Evolutionary Biology, 17: 222. The article is available at: http://hdl.handle.net/1956/17387
Paper III: Georgieva, M. N., Wiklund, H., Bell, J. B., Eilertsen, M. H., Mills, R. A., Little, C. T. S., & Glover, A. G. (2015). A chemosynthetic weed: the tubeworm Sclerolinum contortum is a bipolar, cosmopolitan species. BMC Evolutionary Biology, 15: 1-17. The article is available at: http://hdl.handle.net/1956/12183
Paper IV: Eilertsen, M.H., Georgieva, M.N., Kongsrud, J.A., Wiklund, H., Glover, A.G. Rapp, H.T. (2018) Genetic connectivity from the Arctic to the Antarctic: Sclerolinum contortum and Nicomache lokii (Annelida) are both widespread in reducing environments. Scientific Reports, 8: 4810. The article is available at: http://hdl.handle.net/1956/17714