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The role of phylogenetic relatedness in invasion success: A multidisciplinary study of marine biological invasions

Final Report Summary - MARINVASPHYLOGEN (The role of phylogenetic relatedness in invasion success: A multidisciplinary study of marine biological invasions)

MarInvasPhylogen interfaces disciplines such as community and molecular phylogenetics with ecological and evolutionary interpretations of biological invasions in the sea. Studies merging ecology and genetics have created unprecedented opportunities to integrate both micro- and macro-evolutionary processes in community ecology. This has challenged / advanced a number of fundamental theories in evolution, outlining the importance of the study of phylogenetic relationships among groups to understand ecological and evolutionary processes. Relatedness between introduced and native species can be an important factor in predicting which introduced species will become high-impact invaders in both aquatic and terrestrial ecosystems. The application of the study of phylogenetics to the ecology of invasions is thus of fundamental importance, yet it remains poorly explored in marine environments.
MarInvasPhylogen includes four specific research areas, namely ‘community ecology’, ‘molecular phylogeny’, ‘community phylogenetics’ and ‘morphological phylogeny’. The first three research areas were examined during the outgoing phase of this fellowship at the University of California, Davis (henceforth UC Davis) and integrate disciplines such as community phylogenetics and ecology with molecular studies, in order to assess the role of phylogenetic relationships between invasive and non-invasive marine species. The last research area (i.e. ‘morphological phylogeny’) was addressed during the return phase at the Centre d’Estudis Avançats de Blanes (CEAB - CSIC). Furthermore, during this phase the results obtained during the duration of the project were integrated.
The first part of the project (i.e. ‘community ecology’) involved field surveys as well as both field and laboratory experiments. These experiments were used to obtain a holistic understanding of the forces ruling community assembly and ecological interactions between invasive species and receiving communities. All fieldwork and experiments were carried out along the North Californian coastline, where Prof. Stachowicz has extensive experience and where the facilities of the Bodega Marine Laboratory of UC Davis are located. This work has included two different facets:

1. Field and laboratory experiments to understand how different phyla act as biotic resistance and inhibit the invasive behaviour of a non-indigenous species across its life cycle. Manipulative experiments modifying diversity patterns and densities of both predators and competitors were conducted, as well as monitoring survival, growth and dominance over time. An objective of the project was to study ecological processes that rule the interactions between native and non-indigenous species, and how these interactions influence the success of invasive species. Through this work we have demonstrated that different mechanisms of biotic resistance occur across the life cycle and together limit the invasion success of an introduced marine invertebrate in northern California. The presence of biotic resistance mechanisms acting at multiple life stages, and potentially under different conditions, suggests that different components of biotic resistance interact to enhance the resident community’s resistance to invasion. Considering that the outcome of ecological interactions that underlie biotic resistance might depend heavily on the phylogenetic context in which species interact, our research suggests that studies of biotic resistance that consider single processes, patches, species or life-history stages, provide an incomplete picture of the capacity of communities to resist invasion. Consequently, there is a need to consider a more holistic approach when studying biological invasions such as including the phylogenetic context when assessing species interactions. The results have been published and presented at various international conferences and workshops (see details below).
2. Analysing species distribution and abundance over long periods of time is critical to understand community patterns associated with ecological interactions. The Researcher, Dr. Marc Rius, has studied abundance and phenological patterns of both adults and recruits at three sites of the Bodega harbour using both a short and long-term community dataset covering the period from 2002 until 2011. Dr. Rius performed estimates of occupancy (% cover) and density for all species represented, and analyzed temporal and spatial patterns to understand the role of ecological processes and phylogeny on community structure.

For the second and third part of the project (‘molecular phylogeny’ and ‘community phylogenetics’ respectively), Dr. Rius completed extensive training on phylogenetic tools and had the opportunity for wide-ranging interactions with researchers highly skilled in community and molecular phylogenetics at UC Davis. Molecular data stored in molecular databases (e.g. NCBI GenBank) were collected and new data from species not present in the databases were obtained by sequencing selected genes. Dr. Rius organized sampling trips to collect tissue samples from along the Californian coast (e.g. Santa Barbara, Bodega Bay) to obtain novel sequence data. DNA regions were amplified with a thermal cycler using the polymerase chain reaction. The molecular phylogenetic analyses were conducted using the programmes learned during the training. Dr. Rius conducted alignments of the gene data sets using the programme MEGA and SSU and estimated phylogenetic relationships with Bayesian inference (MrBayes). In addition, Dr. Rius collected trait data on categorical variables such as invasiveness or coloniality, and discrete variables such as the global distribution of each species. Regarding the community phylogenetics analyses, the ecological experimental results provided key information to run such analyses and were integrated with trait data to understand community patterns. Two analyses have been considered: one regional that focused on Californian species, and another global including all possible species.
In summary, the outgoing phase of MarInvasPhylogen has allowed for an extensive diversification of the specialization in marine biological invasions of the researcher, and enabled him to gain important knowledge and experience across a number of exciting and pertinent research fields.
The returning phase of the fellowship focussed particularly on ‘morphological phylogeny’. The aim was to ascertain the congruence among the results found in the study of community phylogenetics, molecular and morphological phylogenies, and community ecology to provide a holistic understanding of the role of phylogenies in invasiveness. Other specific objectives were to determine how phylogenetic relationships affect the ecological interactions among the studied organisms, and ultimately test the relevance of both ecological and phylogenetic forces.
The arrival of invasive marine species is affecting, and will in the future greatly affect, all European coastal areas. The consequences of bioinvasions are becoming increasingly important for human economies (e.g. impacts on aquaculture facilities and fisheries), especially in coastal areas. Consequently, the European Science Foundation has identified the study of biological invasions as a key research area. The findings and techniques developed through the MarInvasPhylogen project will benefit numerous stakeholders, namely coastal managers, municipalities, companies, the tourism industry and other sectors that work with coastal areas across Europe (local, regional, national or European administrations).

Finally, an objective of the Marie Curie International Outgoing Fellowship, namely to reintegrate researchers into the European academic system, has in the case of Dr. Rius, been achieved. He has recently taken up a permanent position as a Lecturer at the University of Southampton, United Kingdom, which prompted the early termination of this Marie Curie IOF duly requested and approved.