Microscopic Stages of North Atlantic Laminaria digitata (Phaeophyceae) Exhibit Trait-Dependent Thermal Adaptation Along Latitudes

Abstract

Kelp forests in the North Atlantic are at risk of decline at their warm temperature distribution margins due to anthropogenic temperature rise and more frequent marine heat waves. To investigate the thermal adaptation of the cold-temperate kelp Laminaria digitata, we sampled six populations, from the Arctic to Brittany (Spitsbergen, Tromsø, Bodø [all Norway], Helgoland [Germany], Roscoff and Quiberon [both France]), across the species’ entire distribution range, spanning 31.5° latitude and 12-13°C difference in mean summer sea surface temperature. We used pooled vegetative gametophytes derived from several sporophytes to approximate the genetic diversity of each location. Gametophytes were exposed to (sub-) lethal high (20-25°C) and (sub-) optimal low (0-15°C) temperature gradients in two full-factorial, common-garden experiments, subjecting subsets of populations from different origins to the same conditions. We assessed survival of gametophytes, their ability to develop microscopic sporophytes, and subsequent growth. We hypothesized that the thermal performance of gametophytes and microscopic sporophytes corresponds to their local long-term thermal history. Integrated gametophyte survival revealed a uniform upper survival temperature (UST) of 24°C among five tested populations (Tromsø to Quiberon). In contrast, following two weeks of thermal priming of gametophytes at 20-22°C, sporophyte formation at 15°C was significantly higher in southern populations (Quiberon and Roscoff) compared to the high-latitude population of Tromsø. Between 0-15°C, survival of the Arctic population (Spitsbergen) was negatively correlated with increasing temperatures, while the southern-most population (Quiberon) showed the opposite. Thus, responses of survival at low, and sporophyte formation at high temperatures, support the concept of local adaption. On the other hand, sporophyte formation between 0-15°C peaked at 6-9°C in the Quiberon and at 9-12°C in the Spitsbergen population. Sporophyte growth rates (GR) both in length and width were similar for Spitsbergen, Tromsø and Quiberon; all had maximum GRs at 12-15°C and low GRs at 0-6°C. Therefore, responses of sporophyte formation and growth at low temperatures do not reflect ecotypic adaptation. We conclude that L. digitata populations display trait-dependent adaptation, partly corresponding to their local temperature histories and partly manifesting uniform or unpredictable responses. This suggests differential selection pressures on the ontogenetic development of kelps such as L. digitata.

Temporal genomics help in deciphering neutral and adaptive patterns in the contemporary evolution of kelp populations

“…In addition, some of these candidate loci have important metabolic and cellular functions that could be involved in adaptive responses. While our findings support the hypothesis that SST is driving the adaptive response of L. digitata, consistent with previous heat stress experiments performed on the same populations (Liesner et al, 2020;Schimpf et al, 2022) and genome scans of other kelp species (Guzinski et al, 2020;Mao et al, 2020;Vranken et al, 2021), it is important to note that confounding factors may also be at play. This is particularly relevant in the present study because of the phylogeographical history of the species along the North Eastern coast of the Atlantic which indicated that L. digitata is composed of two different clusters (Neiva et al 2020).…”

“…Together, these findings support that genetic drift relative to selection is an important component of the contemporary evolution of this population. This is in line with earlier reports, indicating low levels of genetic diversity at microsatellites in Helgoland (Liesner et al, 2020;Fouqueau, 2021) and signals of local adaptation to temperature that became less clear when comparisons have been made with gametophytes from Helgoland rather than Quiberon (Schimpf et al, 2022). Several factors linked to the geographical isolation of the population and frequent high summer temperatures that both reduced or even inhibited the reproduction of individuals and cause severe bottlenecks (Bartsch et al, 2013) are likely to be involved in its genetic impoverishment.…”

“…Given the increasing body of evidence supporting the role of temperature in driving adaptation within the species (King et al, 2019;Liesner et al, 2020;Schimpf et al, 2022) sea surface temperature (SST)…”

“…Understanding the ability of such cold-temperate water species to adapt to warmer conditions is crucial in assessing their vulnerability to local extinction (Araújo et al, 2016;Arafeh-Dalmau et al, 2019;Filbee-Dexter et al, 2020). Recent studies on Laminaria digitata in the Northern Hemisphere have suggested that populations at the south margin may exhibit lower sensitivity to heat stress compared to those in the North (Liesner et al, 2020;Schimpf et al, 2022). Although significant progress has been made in understanding the genetic basis of thermal preference and heat tolerance in kelp species (Mao et al, 2020;Guzinski et al, 2020;Vranken et al, 2021), identifying candidate loci by genome scans for local adaptation at a single time point remains challenging due to pronounced levels of neutral differentiation.…”

Effects of temperature and nutrients on microscopic stages of the bull kelp (Nereocystis luetkeana, Phaeophyceae)

“…Finally, both thermal history and genetic differentiation can cause population‐specific responses to ocean warming (Liesner et al, 2020; Sánchez de Pedro et al, 2022). Kelp responses to warming can depend on previous thermal exposure (Gauci et al, 2022), which tends to differ across populations, leading to intraspecific differences in thermal tolerance (Becheler et al, 2022; Martins et al, 2020; Schimpf et al, 2022; Strasser et al, 2022). The Salish Sea is a large and complex estuarine system, with sea surface temperatures that can span >8°C across sites that are <100 km apart, depending on the tides, currents, river inputs, and distance from the Pacific Ocean (MacCready et al, 2021).…”