Connectivity of larval and juvenile common sole at a small and large spatial scale

Population persistence depends on recruitment during early life. In marine populations, colonization, replenishment and resilience is influenced by connectivity between spawning and nursery grounds. Connectivity, i.e. the successful exchange of individuals between spawning and nursery grounds, is therefore a crucial determinant of successful recruitment. Yet, empirical evidence of connectivity between distinct spawning and nursery grounds is scarce. Connectivity of the early-life stages of marine organisms is complex to explore due to poor knowledge on larval sources and sinks and sampling challenges. Temporal recruitment can be highly variable on small spatial scales. Understanding connectivity, especially at the scale of larval dispersal, is paramount to metapopulation persistence, prompting for the further development of multi-disciplinary approaches. Fisheries research is increasingly conceptually and technically benefiting from the integration of genetic, phenotypic and spatial studies to unravel the evolutionary mechanisms of population structure.

In this thesis, we developed and integrated novel knowledge on the early-life connectivity of a flatfish at the scale of dispersal (5-500 km) with a multi-disciplinary approach. An intensive sampling program on a small geographical scale was conducted to collect juvenile sole Solea solea in the Southern North Sea. Local connectivity was measured by otolith shape, elemental analysis and molecular markers. The information from each of these tools contributed to a specific aspect of the ecological and evolutionary understanding of dispersal throughout the life cycle. Molecular markers were used as individual tracers of movement and as population tracers of gene flow. Otolith shape is a reliable individual phenotypic trait and elemental analysis tracks an individual from close to birth to capture. But more important, the combination of markers sensitive to complementary ecological and evolutionary processes is most promising. The multi-disciplinary approach proved useful to account for the local dynamics involved in the connectivity between spawning and nursery grounds and on the nursery grounds. The findings are meant to calibrate the biophysical models and to contribute to stock management.

Juvenile sole sampled on the nursery grounds of the Southern North Sea were markedly different in otolith chemistry. The differences in elemental composition (especially for the elements Sr, Mg and Zn) suggested that movement following settlement is limited on the nursery ground, while pre-settlement dispersal is likely restricted to about 100 km. Thus, our results suggested a longer dispersal distance before settlement than after settlement, with some but overall few juvenile migrants between nursery grounds. Each sampling region locally recruited uneven proportions of juveniles (0-100%) from four natal sources. This result validated modelling outputs suggesting that a single spawning ground may contribute to several nursery grounds. Evidence for local recruitment, larval dispersal to several neighboring nursery grounds and limited connectivity between nursery grounds of sole in the North Sea can contribute to the calibration of biophysical models, and feedback on scientific advice on fisheries management and the design of marine protected areas.

Despite the limited connectivity between nursery grounds, the level of genetic differentiation of juvenile sole in the North Sea is low. The low genetic differentiation could be explained by limited but significant mixing between the nursery grounds at the juvenile stage, but also by gene flow on the spawning aggregations at the adult stage. Just a few migrants per generation are needed to maintain a high level of gene flow. The low level of successful recruitment of migrants observed with elemental analysis is compatible with the homogeneous population structure of sole in the North Sea as revealed by genetic markers. Yet, there is no evidence of genetically mixed spawning aggregations for sole.

Regardless of high connectivity within the Southern North Sea, some evidence pointed to local structuring of sole. Within nurseries, elemental composition separated the western and the eastern sides of the Belgian nursery which might be explained by inflow from the Western Scheldt influencing water elemental composition. Local differences in putative adaptive markers between cohorts may be linked to selective pressure acting on 0-group sole on the nursery grounds. However, a causal link between molecular diversity and cohort structure would require further research. Provided that a small proportion of adults successfully contributes to the next generation (as predicted by evidence of sweepstake recruitment), local genetic differences may originate from one panmictic spawning aggregation. In addition, kin structure (i.e. settlement of related individuals in the same area) has been detected on the Belgian nursery. Our results suggest, as expected, limited relatedness between individuals which will not influence the Wahlund effect. Testing for chaotic genetic patchiness in sole would require additional sampling. Nevertheless, chaotic genetic patchiness is a common feature of marine organisms.

As highlighted by this study, elemental composition and putatively adaptive genetic markers are of considerable value to understand connectivity in species with extended larval dispersal dynamics and / or low levels of genetic differentiation as it is the case for sole in the North Sea.