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Kelps, the marine forest foundation species, are threatened by ocean warming at their warm distributional edges. To mechanistically investigate inheritance of thermal traits, we assessed thermal tolerance of inbred (selfings) and outbred (crosses) sporophytes of the N-Atlantic kelp Laminaria digitata among isolates from the genetically distinct populations of Helgoland (North Sea) and Spitsbergen (Arctic). First, we investigated the upper thermal tolerance of microscopic sporophytes in a 14-day experiment applying 20–23°C. The upper survival temperature was lower for the Spitsbergen selfing (21°C) than for the Helgoland selfing and the reciprocal crosses (22°C). We then subjected 4–7 cm long sporophytes to a control temperature (10°C), moderate (19°C) and sub-lethal heat stress (20.5°C) to assess metabolic regulation via whole-transcriptome analysis in addition to physiological parameters. Growth and optimum quantum yield decreased similarly in both crosses and the Helgoland selfing at 19 and 20.5°C, while inbred Spitsbergen sporophytes died within seven days at both 19 and 20.5°C. At 10°C, the Spitsbergen selfing showed the highest differential gene expression. Considering only the three surviving lineages at 20.5°C, differential gene expression was 61–78% lower in the crosses compared to the Helgoland selfing, including reduced expression of transcripts related to cellular stress responses. This implies that both intraspecific crosses maintained a growth response similar to the Helgoland selfing with reduced metabolic regulation during sublethal heat stress, indicating subtle heterosis (hybrid vigour) as a beneficial effect of outbreeding. Results are discussed in the frame of mariculture and marine forest restoration.

In recent years, kelp populations worldwide have faced decline and extirpation at their equatorward limits, while models predict a poleward shift of kelp ecosystems during climate change. To gain an understanding of local thermal adaptation and response plasticity in a forest-forming kelp species, we assessed populations of Laminaria digitata along its entire European distribution range for their capacity to withstand high temperature stress, and analysed population structure and diversity with microsatellite markers (n=12). We sampled wild meristematic L. digitata material (n=30) at six locations ranging from Kongsfjorden, Spitsbergen, to the southernmost distribution limit in Quiberon, France. In a heatwave experiment, we subjected samples from all locations to the same, sublethal temperature treatments (15–23°C for eight days including acclimation) and assessed growth, storage compounds, photosynthetic efficiency and pigment contents as response traits. Recovery was assessed following seven days at 15°C. Microsatellite genotyping revealed all sampled populations to be genetically distinct entities, underlying strong regional structuring between southern and northern clades. Genetic diversity was highest at the southern distribution limit in Quiberon and lowest in the geographically isolated population on the island of Helgoland in the North Sea. The physiological response of L. digitata to temperature was similar over the entire distribution range and did not reflect the mean temperature gradient along the latitudinal gradient. However, material from Spitsbergen and Helgoland presented subtle differentiations in their temperature responses, which reflect long-term local temperature histories at these sites. Finally, a heatwave reaching 23°C for five days led to a cessation of growth, from which none of the sampled populations recovered. Our results suggest that the heat stress response of L. digitata is generally stable across its distribution range, despite strong genetic structuring of the populations. Slight local differentiation occurred in populations from the most distinct thermal environments, but 23°C posed a growth limit for all populations. This implies that local adaptation in trailing edge populations of L. digitata might not alleviate detrimental effects of global warming.