Description: The plasticity of different kelp populations to heat stress has seldom been investigated excluding environmental effects due to thermal histories, by raising a generation under common garden conditions. Comparisons of populations in the absence of environmental effects allow unbiased quantification of the meta-population adaptive potential and resolution of population-specific differentiation. Following this approach, we tested the hypothesis that genetically distinct arctic and temperate kelp exhibit different thermal phenotypes, by comparing the capacity of their microscopic life stages to recover from elevated temperatures. Gametophytes of Laminaria digitata (Arctic and North Sea) grown at 15˚C for 3 years were subjected to common garden conditions with static or dynamic (i.e., gradual) thermal treatments ranging between 15 and 25˚C and also to darkness. Gametophyte growth and survival during thermal stress conditions, and subsequent sporophyte recruitment at two recovery temperatures (5 and 15˚C), were investigated. Population-specific responses were apparent; North Sea gametophytes exhibited higher growth rates and greater sporophyte recruitment than those from the Arctic when recovering from high temperatures, revealing differential thermal adaptation. All gametophytes performed poorly after recovery from a static 8-day exposure at 22.5˚C compared to the response under a dynamic thermal treatment with a peak temperature of 25˚C, demonstrating the importance of gradual warming and/or acclimation time in modifying thermal limits. Recovery temperature markedly affected the capacity of gametophytes to reproduce following high temperatures, regardless of the population. Recovery at 5˚C resulted in higher sporophyte production following a 15˚C and 20˚C static exposure, whereas recovery at 15˚C was better for gametophyte exposures to static 22.5˚C or dynamic heat stress to 25˚C. The subtle performance differences between populations originating from sites with contrasting local in situ temperatures support our hypothesis that their thermal plasticity has diverged over evolutionary time scales.

Description: Kelp beds worldwide are under pressure from ongoing climate and environmental change. Along European coastlines increases in seawater temperature and changes in nutrient conditions occur where upwelling events are disrupted and also along eutrophicated coasts. In addition, seaweed responses to change may interact with seasonal daylength cycles. We performed a factorial experiment to examine the combined effects of seawater temperatures, nutrient regimes, and photoperiod (long and short days) in order to better understand how latitudinal or seasonal differences in daylengths affects the sensitivity of transient microscopic kelp stages of Laminaria digitata from the North Sea, to warming and eutrophication. While the optimal temperature range for vegetative gametophyte growth was 10-18ºC under long summer photoperiod conditions, gametogenesis was induced at lower temperatures between 5 and 15ºC, with maximum sporophyte development under long photoperiods and enriched nutrient regimes, which represents local late spring conditions. Although gametogenesis was fastest at 10-15ºC, sporophyte recruitment was highest at 5ºC. As these particular early life cycle processes in L. digitata have different temperature optima, this may drive the seasonal cycle of recruitment in the field. Increasing summer temperatures due to global warming will increase gametophyte size due to enhanced vegetative growth and inhibition of gametogenesis. This will probably lead to delayed but enhanced recruitment of new sporophytes under cooler autumn to spring conditions over a wide geographical scale, preventing the formation of juvenile sporophytes under stressful summer conditions and possibly changing annual recruitment patterns.

Description: Kelp forests are important habitats in the strongly environmentally and seasonally variable Arctic. There is a critical lack of knowledge about how seasonal conditions and climate change scenarios influence survival and reproduction of kelp early life stages. To better understand the regulation of kelp life cycle processes in this harsh environment we focused on the physiological performance and reproductive success of early life stages in Alaria esculenta and Laminaria digitata from Kongsfjorden, Spitsbergen. Gametophyte growth and survival during Arctic winter and subsequent sporophyte recruitment under spring conditions were investigated. Winter conditions (2°C, complete darkness) halted gametophyte growth and prevented the onset of gametogenesis in both species. The gametophytes of L. digitata but not A. esculenta became fertile after returning to spring conditions, suggesting that sporogenesis, sexual reproduction and recruitment in A. esculenta must occur successively during summer/autumn while in L. digitata a new generation of sporophytes could develop from overwintering gametophytes. The effects of simulated canopy shading (offering protection against extreme irradiance stress, particularly as sea ice retreats), present-day and projected Arctic summer seawater temperatures, and nutrient levels on gametophyte survival, fertility and sporophyte recruitment success were also investigated in both species. A. esculenta gametophytes had greater survival and reproductive success than L. digitata, except under very low light (simulating dense canopy). In contrast, shading was required for reproductive success in L. digitata gametophytes. Predicted summer temperatures of 9°C reduced sexual reproduction in both species. Interactions observed between these environmental drivers probably reflect species-specific seasonal patterns of survival and reproduction. These differences between kelp species in response to abiotic factors and light levels (simulated canopy shading) suggest that climate change could alter community structure in the Arctic through effects on sexual reproduction and sporophyte recruitment success.

Description: In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.

Description: Many organisms have endogenous clocks that synchronize biological processes with environmental changes, leading to optimized development and reproduction. However, certain environments, like the Arctic, pose a special challenge to circadian clocks, particularly due to extreme seasonal changes in daylength, ranging from permanent sunlight to complete darkness. Kelps seem to be well adapted to the variable environmental conditions characteristic of this region. However, daylength might affect kelp species that use circadian rhythms to control the timing of daily egg release from female gametophytes. We aimed to investigate how daylength and light intensity affect gametogenesis and reproductive success of summer-reproducing kelp species (using Alaria esculenta as a model). As daylength and temperature co-vary most of the year, we also investigated the thermal resilience of the sporophytes developed under different daylengths to understand if there is a cross-tolerance between light doses and temperature tolerance. Although continuous daylight, characteristic of Arctic summers, enhanced gametogenesis and increased gametophyte vegetative growth, and thereby the number of potential reproductive gametophyte cells, sporophyte production was higher under long (16 h light:8 h dark) and intermediate (12:12 h) days. Sporophyte growth was triggered by changing daylength from short to long days, suggesting a synchronization with annual daylength variation. High daily light doses during reproduction and early development improved subsequent sporophyte survival at high (sub)lethal temperatures, indicating cross-tolerance between light and temperature. Reproductive success in Arctic A. esculenta was hampered under continuous light, and we hypothesize that this might result from disturbance of synchronized egg release and subsequent fertilization.

Description: Thermal characteristics of kelp species have been studied in many ways, but potentially persistent effects of temperature across generations are yet poorly understood. In this context, the effect of thermal priming on fertility and growth of the N-Atlantic kelp species Laminaria digitata was investigated within and across life cycle generations in a two-step common garden experiment. Using vegetative clonal gametophytes from cold (5°C) and warm (15°C) pre-experimental cultivation (3 years), we first quantified gametogenesis and recruitment over two weeks at a common temperature of 10°C. Then, recruited sporophytes were transferred to a temperature gradient spanning the tolerance range of the species from 0°C to 20°C. We hypothesized that a warm gametophyte preexperimental cultivation promotes performance of sporophytes at warm temperatures and vice versa. Interestingly, gametogenesis speed and sporophyte recruitment were higher in gametophytes following cold compared to warm pre-experimental cultivation, which indicates carry-over effects of temperature within the gametophyte generation. Compared to warm pre-experimental cultivation of gametophytes, a cold preexperimental cultivation enhanced growth of juvenile Laminaria digitata sporophytes by more than 69% at the extreme low and high temperatures of 0 and 20°C. This is the first evidence for a cross-generational effect between gametophyte parents and offspring sporophytes. As cold gametophyte cultivation increased the trait performance of gametogenesis, recruitment and thermal tolerance of juvenile sporophytes, priming of early life cycle stages may be used to increase resilience and productivity of kelps in marine forest restoration efforts and kelp mariculture.

Description: Kelps are globally important bioengineering species with high ecological and economic value, but are increasingly threatened by climate-driven geographic range shifts. The inheritance of economically important traits from parents to offspring is poorly understood in kelps but it is of utmost interest to seaweed farmers wishing to select strains with superior performance and resilience to environmental change. For two allopatric kelp species (N-Atlantic Laminaria digitata and S-Atlantic L. pallida), we compared the speed of gametogenesis and reproductive success in parental gametophytes, and produced intraspecific and reciprocal interspecific crosses of female × male gametophyte parents isolated from the two species. We then compared the upper thermal resilience of microscopic and macroscopic sibling sporophytes in an exposure experiment over two weeks. The upper thermal limit of the sporophytes resulting from intraspecific crosses of the two species deviated by 1°C. In contrast, sporophytes from both interspecific hybrid crosses had a 2–3°C higher upper thermal tolerance than single species sporophytes, indicating heterosis for thermal tolerance. This phenotypic esponse appears partially sex-dependent in our study, with female parents being more important in determining the thermal-response phenotype than male parents. The presence of male gametophytes generally enhanced female reproductive success. Both gametogenesis rate and reproductive success differed among the types of reciprocal crosses. Although the interspecific crosses were artificial in an ecological sense, they may provide a tool for understanding the molecular basis of heterosis and thermal tolerance in kelps (e.g. by investigating species-specific gene expression), or for aquaculture breeding programmes against a background of rapid environmental change.