Publications

The study of evolutionary mechanisms that shape the divergence continuum whereby populations diverge, adapt to new environments, accumulate reproductive barriers to gene flow and evolve into new species, is a central topic in evolutionary biology. With the arrival of new sequencing techniques, we have the opportunity to advance our knowledge within this field, as well as to ask and answer fundamental research questions previously impossible to explore. While previous decades of research mainly relied on specific case studies with relatively few model species, comparative frameworks are now commonly used to understand the divergence continuum and to derive general patterns behind divergence processes.
This PhD thesis provides an insight into the evolutionary history involved during the divergence process of populations in marine fishes. These species are often characterised by their ability to disperse, with larvae drifting with ocean currents for several weeks, and their large population sizes, which together result in limited population structure. As such, these species provide interesting models to study the role of evolutionary forces promoting population divergence, for example linked to demographic histories or local environmental adaptations.
The North Sea – Baltic Sea transition zone is an ideal framework to study these evolutionary forces, as the Baltic Sea was connected to the Atlantic Ocean only 8 000 years ago, and presents steep environmental gradients (e.g. salinity) along the transition zone. This environmental gradient is associated with major breaks in the population genetic structure of several marine species. Yet, little is known about the demographic history and the genomic architecture that underlie population divergence and adaptation to this environment in marine fishes. The main goal of this PhD was to fill this knowledge gap by using a comparative population genomics approach on several marine flatfishes that have colonized the Baltic Sea. We found that this colonization was associated with a diversity of divergence patterns, with heterogeneous signals of divergence found across the genome of each species, but also in the genomic architecture of the divergence across species. Therefore, the populations from the North Sea and the Baltic Sea appear to have diverged through species-specific factors. Nevertheless, the presence of ancient lineages and ancient standing genetic variation seem to have fuelled the local adaptation of these species during the colonization of the Baltic Sea.

Marine ecosystems are exposed to a multitude of environmental and anthropogenic pressures, such as overfishing, habitat loss, invasive species and global warming. Such pressures alter the structure and biodiversity of natural communities, thereby potentially affecting the functions and services that marine ecosystems provide, such as food and coastal protection. The goal of ecosystem-based management is to sustainably make use of marine ecosystems whilst protecting its health and functioning. This requires knowledge on how natural communities respond to the range of environmental and anthropogenic pressures. The trait-based approach may provide such knowledge and understanding. It is based on the traits that species carry, which determine which environments a species can inhabit and how it may respond to disturbances. A trait can be any characteristic that one can measure on an organism, and can be related to its behaviour, morphology, life history or physiology. Moreover, characterizing natural communities in terms of their traits allows for comparing ecosystems with entirely different species compositions, thereby enhancing the possibility of finding general patterns across communities and ecosystems. In this thesis I applied a trait-based approach to marine fish communities with the aim to understand how they are structured in terms of traits, and to use traits to assess how fish communities respond to changes in environment and fishing pressure. The response of a community to a change in environment or an anthropogenic disturbance can be detected by investigating shifts in the mean trait values expressed by the community. The North Sea fish community has a history of intense fishing pressure, as well as climate-driven changes during the last few decades. Furthermore, there are strong spatial gradients in environmental conditions, from the shallow, southern parts to the deeper, northern parts where the North Sea meets the North Atlantic. We therefore explored if the North Sea fish community shifted in its mean trait values over time, as well as in space, and if this could be explained by the environment and fishing effort. The community showed a strong temporal shift in its trait composition from large, slow-growing, late-maturing and long-living mean trait values to smaller, faster-growing, earlier-maturing and shorter-living ones. Although the high historical fishing pressure on large species, such as Atlantic cod, and the consequent decrease of such species likely contributed to these shifts, we found that they could also be explained by the increases in temperature, salinity and phytoplankton biomass. However, the temporal changes over time were not the same throughout the area, with some areas showing no shift in community trait means. Moreover, the trait composition of the community varied strongly in space, following the gradients in temperature, seasonality and depth. Our results demonstrated that traits can be used to assess how marine fish communities are structured in space and respond to environmental changes over time, and emphasize the importance of taking both spatial and temporal dimensions of marine fish communities into account. In order for the trait-based approach to be useful in predictive models, it is important to test the generality of the empirical relationships between traits and environment, and to identify which traits respond most strongly to which environmental variables. We therefore combined data on fish communities from the North Atlantic and Northeast Pacific, including >1,200 species, that cover large latitudinal and environmental gradients. We found that particularly traits related to the fast-slow continuum, i.e. age at maturity, lifespan and the growth coefficient K, varied most strongly with environment. Hence, warm, shallow and seasonal waters were associated with fast-growing, early-maturing and short-living species, whereas cold, deep and stable waters were mostly inhabited by slow-growing, late-maturing and long-living species. When using the observed trait-environment relationships to project the trait composition of marine fish communities worldwide, we found that traits were following both large-scale latitudinal gradients in temperature, as well as local coastal-offshore gradients in depth and seasonality. Given the consistent patterns observed across areas with entirely different species composition our results indicate that these general trait-environment relationships of marine fish may prove useful to predict changes in marine fish communities over time. Besides knowing how communities are structured in terms of traits, it may provide additional insight to identify the underlying community assembly processes that lead to the observed structure and composition of marine fish communities. Potential community assembly processes could be related to both biotic and abiotic factors. In this thesis, we studied community assembly of marine fish for the first time at a large spatial scale by assessing if the variation in traits within communities was different from random. Some communities were found to be strongly shaped by the environment that acted as a filter by only selecting species with a particular set of traits. For instance, high temperatures filtered out species with a large size and a long lifespan. Several communities were also found to be shaped by biotic interactions, as observed from the high variation in fecundity and offspring size, suggesting that multiple reproductive strategies can coexist within the same community. However, the majority of communities seemed to be randomly assembled, suggesting that both processes may act simultaneously, thereby cancelling each other out, or that stochastic processes like dispersal and immigration/emigration are more important. The strength at which the observed assembly processes were operating varied moderately with environment, particularly with temperature and depth, but not with fishing pressure and primary production. Further knowledge on potential other community assembly processes acting on marine fish and the inclusion of intraspecific trait variation are needed to fully understand the underlying mechanisms of marine fish communities are assembled. This thesis demonstrated that the structure of marine fish communities is strongly linked to the environment by acting on the trait composition of communities – both in space and time, as well as at small and large spatial scales. We identified key response traits and trait-environment relationships for marine fish that should be further explored and tested in other types of ecosystems. This thesis will hopefully inspire future research to create predictive models that can explore how marine fish communities may change under global warming, in combination with fishing, and to inform ecosystem-based management on the expected changes to come. This will allow users of marine ecosystems to adapt and to continue to benefit from the services provided by marine ecosystems in the future.

With the reform of the European Union (EU) Common Fisheries Policy and the implementation of the Landing Obligation the ability of the fishing industry to adjust the selectivity of their gears is more than ever important in determining the revenue of fisheries. This is due to the change from landings- to catch-based fisheries management, where unwanted catches of regulated species now have to be landed and counted against the quota. Moreover, as the quantity and composition of unwanted catch varies with type of fishing gear used, fishing areas, season, fishing practice and quota availability, changes to the selectivity of the gears will be needed at the vessel level. This implies that a larger number of specialized selective gears need to be available to the different fisheries. Such an extensive development and testing of selective gears is difficult to achieve under the traditional process for gear development under the current EU fisheries management system. Therefore, this study investigates the potential of an industry-led process for identifying issues, and for development and testing of gear solutions as a way to provide the necessary tool-box of more specialized gears. Having industry lead the gear development process allows testing numerous fishing gears in parallel, as well as establishing a real commercial development and testing phase prior to expensive scientific trials. Moreover, this parallel development of different gear solutions allows for quickly filtering the most promising ones. Key steps of such an industry-led gear development process were investigated during this study, such as the possibility for industry to collect selectivity data on the gears tested, or what type of gears can this process produce. This PhD thesis consists of a synopsis and four papers.

The marine habitat is a major component of the Earth System with the oceans covering 70% of earth's surface, and for physical as well a biological reasons the oceans play a major role in global climate. Biologic activities in the oceans draw down 48.5 Gt C from the atmosphere every year, whereof up to 25% of this carbon is transported out of the photic zone via the biological carbon pump. Even though it is a small fraction of this that is sequestered at depth (1-3%), it underlines the huge potential of the marine biota to impact and shape global climate, both in the past, present and future ocean. The current anthropogenic climate change is, among other things, predicted to alter ocean circulation, stratification and nutrient availability in the marine environment, all three aspects that play a crucial role for marine biota with feedback on global climate. For this reason, it is crucial to improve our understanding of the functioning of marine ecosystems in relation to environmental (abiotic and biotic) variability gradients. As primary producers, planktonic organisms are a key compartment and energetic pathway that link resource availability to marine food webs. As such, the planktonic community play a central role in biogeochemical cycles in the ocean in general and production and export in particular.
The trait based approach forms the base of the studies in my thesis, as it is ideal to provide simple models of the individual organisms and their interaction with each other and the environment. Using this approach we create a link between
performance traits of organism and the actual ecological niches in space and time in which they dominate, and nd a general resemblance of our predictions with observations. The success of the trait based approach in relation to my studies is taking the step from predicting under which conditions a certain trait combination is optimal, to exploring how biomass of organisms showing these specific traits evolve in a dynamic seasonal cycle.
In this thesis I quantify and systematize two important aspects of marine plank-tonic life that influence the export and sequestration of carbon to the sea floor: the phenomena of diel vertical migration (DVM) in zooplankton and the general success of diatoms in seasonal environments.
DVM is a strategy among zooplankton such as calanoid copepods to increase the chance of survival and hence their fitness. Their presence in the sunlit ocean surface attracts predators, and to decrease this predation risk many zooplankton
individuals migrate to darker depths during the day. Consequently these migrators feed predominantly during night, when they reside in the surface layers. Besides the immediate decrease in predation risk, the migrating zooplankton faces a lost feeding opportunity, by abandoning the productive surface layer for a large part of the day. The question of DVM hence becomes a question of a trade-off between costs and benets; zooplankton have to balance costs of lost feeding opportunity and swimming expenditure to the benet of reduced predation risk, factors that vary with size of the zooplankter, availability of food and degree of illumination of the water column. Along with respiration, some of the food that is consumed in the surface is later excreted at depth, which has been proposed as an enhancing effect on the carbon export, and hence adds an active component to the biological carbon pump. Using a model estimate of food abundance in the surface layers we predict that 16-30 % of the carbon exported in the North Atlantic might be mediated by diel vertically migrating zooplankton. Indeed this number might also be influenced by the type of diet the zooplankton consumes; an increase in fecal pellet production and density is observed in copepods feeding on diatoms.
In the modern ocean, diatoms are responsible for as much as 50 % of carbon exported via the biological carbon pump, and hence they have a crucial role in ecosystem functioning with feedback to global climate. Their special physiology is
characterized by a silica exo-skeleton and a large water-filled, central vacuole, and their dominance in marine ecosystems are widespread in nutrient rich, upwelling areas. The lifestyle of diatoms is in several ways filled with dichotomies; they rely on a nutrient that they themselves deplete, they build a heavy shell, that they have to counter act with buoyancy and the protection that the shell aords seems to be at odds with the conspicuous success of diatoms in grazer -poor environments. We take a mechanistic approach to illuminating the success of diatoms and find that their special physiology leads to several advantages strongest in nutrient-rich spring- like conditions. Our results underscore the grazing pressure as the main driver for vacuolation.
The succession of diatoms and mixotrophs cover most of the phytoplankton community's strategies with regards to acquiring nutrients, from the strictly autotroph diatoms to heterotrophic dinoflagellates. The last part of my thesis sets up a competition experiment modelling the strategies of vacuolation as opposed to mixotrophy, and examines how the optimal strategies evolve in terms of abundance in the seasonal cycle. From the unification of these two types in a dynamic seasonal cycle there emerges a realistic succession pattern of large, highly vacuolated diatoms in spring superseded by a community of small diatoms and mixotrophs coexisting with large heterotrophs in the nutrient depleted summer. This emphasizes the propagation of nutrient-rich, well mixed ocean environment as a prerequisite for the continued success of diatoms in the future ocean.