Aim The life cycle of many organisms is all but fixed across their distribution range. Most commonly, populations respond to environmental variation by shifting the timing of reproductive events (phenology). More profoundly, populations may (partly) shift their mode of reproduction from sexual to asexual. Life cycle variation can impact reproductive success, gene flow, genetic diversity and, ultimately, the evolutionary trajectory of populations. Understanding the factors that influence life cycle variation is essential for grasping the biology and ecological roles of species. This study investigates the variation in life cycles and its effects on the genetic diversity of a brown seaweed, Dictyota, across its European range.Location North-East Atlantic Ocean and the Mediterranean Sea.Taxon Dictyota dichotoma (Hudson) J.V. Lamouroux (Phaeophyceae, Dictyotales).Methods We monitored phenology, fertility and lifespan in Atlantic and Mediterranean populations at its northern and southern boundaries and used microsatellite markers to assess how these factors influence genetic and genotypic diversity.Results We observed significant differences in phenology, reproductive strategies and genetic diversity among northern and southern European populations. In Mediterranean populations, D. dichotoma exhibited sporophytic dominance with gametophytes being extremely rare, suggesting a shift towards asexual reproduction. In contrast, North-East Atlantic populations displayed more pronounced seasonal reproductive patterns with higher frequencies of gametophytes, indicating predominant sexual reproduction. However, genetic analysis showed lower allelic richness and unique alleles in northern populations, whereas southern populations were genetically more diverse, reflecting historical biogeographic processes. Clonal reproduction was more pronounced in the Mediterranean populations, influencing the spatial genetic substructure and contributing to locally lower genotypic diversity compared to Atlantic populations.Main Conclusions Our findings demonstrate that life cycle variation and phenology in D. dichotoma are closely tied to regional environmental conditions and have significant implications for population structure and genetic diversity. Results highlight how shifts in reproductive strategies contribute to the evolutionary and ecological dynamics of marine macroalgae across biogeographical gradients.
Abstract As one of the earliest-diverging multicellular eukaryotic lineages, the bladed Bangiales (Rhodophyta) possess a deep evolutionary history with a central role in the multi-billion-dollar global seaweed aquaculture industry. Although North Atlantic representatives are emerging candidates for regional mariculture, the scarcity of high-quality genomic resources for these taxa hinders both fundamental research and commercial optimization. To address this, we present the first chromosome-level genome assemblies for two native European species: Porphyra dioica (150.44 Mbp) and Porphyra linearis (95.22 Mbp). By integrating Oxford Nanopore Technologies (ONT) long-read sequencing with Hi-C proximity ligation, we generated highly contiguous nuclear genomes resolved into five chromosomes. Structural gene models were predicted through the BRAKER3 pipeline, identifying 12,548 and 10,382 protein-coding genes for P. dioica and P. linearis , respectively. Subsequent homology-based functional annotation characterized 57.4% and 59.8% of these predicted proteins. Supplemented by circularized organellar genomes, these reference genomes provide a critical framework for future research, enabling comparative studies of Atlantic-Pacific divergence and facilitating the development of selective breeding programs for sustainable European aquaculture.
Kelp forests are among the most extensive and productive coastal ecosystems, yet they remain underrepresented in global conservation policy despite widespread declines driven by interacting global- (i.e., ocean warming, marine heatwaves) to local-scale stressors. At the same time, kelp conservation and restoration efforts are expanding rapidly across regions, but measures of success and syntheses tend to primarily focus on ecological conditions and trends, not on conservation and restoration actions. To fill this gap, we developed a comparative global dataset of kelp conservation initiatives based on expert-derived regional narratives from 209 participants spanning 35 regions with kelp forests. We applied a structured presence–absence scoring framework across six domains: conservation actions, restoration approaches, governance actors, conservation objectives, social dimensions, and funding structures, supplemented by regional expert knowledge to enable cross-regional comparison. Across regions, conservation was characterised by strong emphasis on monitoring (86
BACKGROUND:Kelp forests are among the most productive and biodiverse ecosystems on Earth, yet they are currently facing unprecedented degradation and decline. In Europe, the conservation of these key ecosystems has historically relied on a plethora of disconnected national policies and passive protection, and they have frequently been underrepresented in governance frameworks. The recent adoption of the European Union Nature Restoration Regulation (NRR) represents a transformative shift, establishing the first legally binding targets for large-scale conservation and restoration of marine ecosystems shared by European Union members. SCOPE:Here, we discuss the challenges and opportunities that the NRR presents for European kelp forests and associated ecosystem services across Europe. As the NRR sets ambitious mandates for mapping habitats, condition assessments, and restoration by 2030-2050, its success depends on overcoming existing data gaps as well as on financial and technical challenges. We highlight how the NRR provides a valuable instrument to initiate immediate action across regions, and we propose a set of priority actions to achieve the NRR targets and address current scientific gaps. CONCLUSIONS:We emphasize the need for transboundary harmonization of monitoring protocols and methods for establishing reference areas for healthy kelp forests, the development of high-resolution maps for habitat distribution and condition, the establishment of clear-cut criteria for identifying resilient restoration areas (i.e., priority sites capable of achieving and maintaining favourable conservation status under NRR targets), and the development of standardized condition indicators (e.g., canopy density, indicator species) to assess "good condition" across different ecoregions. By linking legal requirements with science-based strategies, the NRR provides an opportunity to finally integrate kelp forests into European marine governance and achieve long-term sustainability for these critical ecosystems.
The genus Dictyota includes ecologically important brown seaweed species that, apart from contributing to the foundation of the marine ecosystem, are gaining traction for their economic value. Substantial research has focused on taxonomy, chemical composition, ecological roles, and economic potential of Dictyota, including studies on genetics and genomics. Here, we developed twelve novel microsatellite markers for Dictyota dichotoma by using Ion Torrent sequencing. The markers were tested using 50 diploid individuals collected from five natural populations of D. dichotoma. The number of alleles per locus varied between five and thirteen. The total heterozygosity ranged from 0.587 to 0.887 per locus, and from − 0.147 to 0.483 in five populations across its European range. These polymorphic microsatellite markers are valuable for studying population genetic diversity and differentiation in D. dichotoma and may also be beneficial for other genetic research related to the reproductive biology of this model species, which displays considerable variation across the species’ range.
The resilience of populations to extreme climatic events comprises the resistance to withstand and the ability to recover, which depends on factors such as remaining genetic diversity and population connectivity. In 2011, a MHW caused a 100 km range contraction of kelp (Ecklonia radiata) off Western Australia, but recently recovering kelp forests were discovered. To understand mechanisms of recovery and determine if recovering populations are survivors or immigrants, we used genotyping-by-sequencing to assess patterns of genetic diversity and connectivity. We found that two of the three recovering kelp forests (PG1 and 2) were likely survivors whereas a third smaller population (PGCr 1) was likely produced through re-colonisation from nearby surviving forests. Connectivity was high among populations and migration analysis identified one population (Horrocks) as the most important source for the recovering kelps. All recovering populations had higher neutral genetic diversity, and similar putative adaptive diversity to surrounding surviving populations, suggesting local adaptation. Our results elucidate how mixed processes can contribute to kelp forest resilience following MHWs but cryptic survival and maintenance of population connectivity is key to recovery.
Ongoing and predicted range loss of kelp forests in response to climatic stressors is pressing marine managers to look into the adaptive capacity of populations to inform conservation strategies. Characterising how adaptive genetic diversity and structure relate to present and future environmental variation represents an emerging approach to quantifying kelp vulnerability to environmental change and identifying populations with genotypes that potentially confer an adaptive advantage in future ocean conditions. The dominant Australian kelp, Ecklonia radiata, was genotyped from 10 locations spanning 2000 km of coastline and a 9.5°C average temperature gradient along the east coast of Australia, a global warming hotspot. ddRAD sequencing generated 10,700 high-quality single nucleotide polymorphisms (SNPs) and characterized levels of neutral and adaptive genomic diversity and structure. The adaptive dataset, reflecting portions of the genome putatively under selection, was used to infer genomic vulnerability by 2050 under the RCP 8.5 scenario. There was strong neutral genetic differentiation between Australia mainland and Tasmanian populations, but only weak genetic structure among mainland populations within the main path of the East Australian Current. Genetic diversity was highest in the center of the range and lowest in the warm-edge population. The adaptive SNP candidates revealed similar genetic structure patterns, with a spread of adaptive alleles across most warm (northern) populations. The lowest, but most unique, adaptive genetic diversity values were found in both warm and cool population edges, suggesting local adaptation but low evolutionary potential. Critically, genomic vulnerability modeling identified high levels of vulnerability to future environmental conditions in Tasmanian populations. Populations of kelp at range edges are unlikely to adapt and keep pace with predicted climate change. Ensuring the persistence of these kelp forests, by boosting resilience to climate change, may require active management strategies with assisted adaptation in warm-edge (northern) populations and assisted gene flow in cool-edge (Tasmania) populations.
A corrigendum doesn’t have an abstract.
A fundamental question in holobiont biology is the extent to which microbiomes are determined by host characteristics regulated by their genotype. Studies on the interactions of host genotype and microbiomes are emerging but disentangling the role that host genotype has in shaping microbiomes remains challenging in natural settings. Host genotypes tend to be segregated in space and affected by different environments. Here we overcome this challenge by studying an unusual situation where host asexual (5 clonal lineages) and sexual genotypes (15 non-clonal lineages) of the same species co-occur under the same environment. This allowed us to partition the influence of morphological traits and genotype in shaping host-associated bacterial communities. Lamina-associated bacteria of co-occurring kelp sexual non-clonal (Ecklonia radiata) and asexual clonal (E. brevipes) morphs were compared to test whether host genotype influences microbiomes beyond morphology. Similarity of bacterial composition and predicted functions were evaluated among individuals within a single clonal genotype or among non-clonal genotypes of each morph. Higher similarity in bacterial composition and inferred functions were found among identical clones of E. brevipes compared to other clonal genotypes or unique non-clonal E. radiata genotypes. Additionally, bacterial diversity and composition differed significantly between the two morphs and were related with one morphological trait in E. brevipes (haptera). Thus, factors regulated by the host genotype (e.g. secondary metabolite production) likely drive differences in microbial communities between morphs. The strong association of genotype and microbiome found here highlights the importance of genetic relatedness of hosts in determining variability in their bacterial symbionts.
The analysis of biological and ecological traits has a long history in evolutionary and ecological research. However, trait data are often scattered and standardised terminology that transcends taxonomic and biogeographical context are generally missing. As part of the development of a global trait database of marine species, we collated trait information for European seaweeds and structured the data within the standardised framework of the World Register of Marine Species (WoRMS). We collected 45 175 trait records for 21 biologically and ecologically relevant traits of seaweeds. This resulted in a trait database for 1745 European seaweed species of which more than half (56 %) of the records were documented at the species level, while the remaining 44 % were documented at a higher taxonomic level and subsequently inherited at lower levels. The trait database for European seaweeds will serve as a foundation for future research on diversity and evolution of seaweeds and their responses to global changes. The data will contribute to developing detailed trait-based ecosystem models and will be an important tool to inform marine conservation policies. The data are publicly accessible through the AlgaeTraits portal, https://doi.org/10.14284/574 (AlgaeTraits, 2022).
Effective monitoring of non-indigenous seaweeds and combatting their effects relies on a solid confirmation of the non-indigenous status of the respective species. We critically analysed the status of presumed non-indigenous seaweed species reported from the Mediterranean Sea, the Northeast Atlantic Ocean and Macaronesia, resulting in a list of 140 species whose non-indigenous nature is undisputed. For an additional 87 species it is unclear if they are native or non-indigenous (cryptogenic species) or their identity requires confirmation (data deficient species). We discuss the factors underlying both taxonomic and biogeographic uncertainties and outline recommendations to reduce uncertainty about the non-indigenous status of seaweeds. Our dataset consisted of over 19,000 distribution records, half of which can be attributed to only five species (Sargassum muticum, Bonnemaisonia hamifera, Asparagopsis armata, Caulerpa cylindracea and Colpomenia peregrina), while 56 species (40%) are recorded no more than once or twice. In addition, our analyses revealed considerable variation in the diversity of non-indigenous species between the geographic regions. The Eastern Mediterranean Sea is home to the largest fraction of non-indigenous seaweed species, the majority of which have a Red Sea or Indo-Pacific origin and have entered the Mediterranean Sea mostly via the Suez Canal. Non-indigenous seaweeds with native ranges situated in the Northwest Pacific make up a large fraction of the total in the Western Mediterranean Sea, Lusitania and Northern Europe, followed by non-indigenous species with a presumed Australasian origin. Uncertainty remains, however, regarding the native range of a substantial fraction of non-indigenous seaweeds in the study area. In so far as analyses of first detections can serve as a proxy for the introduction rate of non-indigenous seaweeds, these do not reveal a decrease in the introduction rate, indicating that the current measures and policies are insufficient to battle the introduction and spread of non-indigenous species in the study area.
Kelp forests are experiencing substantial declines due to climate change, particularly ocean warming and marine heatwaves, and active interventions are necessary to halt this decline. A new restoration approach termed “green gravel” has shown promise as a tool to combat kelp forest loss. In this approach, substrata (i.e. small gravel) are seeded with kelp propagules, reared in controlled conditions in the laboratory before out-planting to degraded reefs. Here, we tested the feasibility of cultivating Australia’s dominant kelp, Ecklonia radiata on green gravel with the aim of optimising the seeding conditions for E.radiata . We seeded substrata (i.e. gravel), that had different surface texture and size, with E. radiata gametophytes at two average seeding densities: high density of ~230 fragments mL -1 and low density of ~115 fragments mL -1 . The tested substrata were small basalt, large basalt, crushed laterite and limestone. Gametophytes successfully adhered to all four tested substrata, however, gametophytes that adhered to the limestone gravel (the natural reef type off Western Australia) suffered extreme tissue bleaching likely due to dissolution and decrease in seawater pH. Gametophytes that adhered to the three other test substrata were healthy, fertilised following seeding and microscopic sporophytes were observed attaching to the gravel. Substrata and seeding density did not affect sporophyte growth (i.e. length) at the time of transferring into aquarium tanks (after three months of rearing in incubators) but over time substrata showed a significant effect on maximum lengths. After 12 months in aquarium tanks, sporophytes on both small and large basalt gravel were significantly larger than those on the crushed laterite. Gametophytes were also found to not only survive on the gravel itself but also detach from the gravel, settle successfully, fertilise and develop into healthy sporophytes ex situ on the surrounding substratum through lateral transfer. Substrata had a significant effect on density of detached gametophytes with rougher and larger gravel showing higher densities of detachment. Our results show the potential for green gravel to be a vector of dispersal for restoration in Western Australia where natural recovery of kelp forests has failed.
Abstract Temperate reefs are increasingly affected by the direct and indirect effects of climate change. At many of their warm range edges, cool‐water kelps are decreasing, while seaweeds with warm‐water affinities are increasing. These habitat‐forming species provide different ecological functions, and shifts to warm‐affinity seaweeds are expected to modify the structure of associated communities. Predicting the nature of such shifts at the ecosystem level is, however, challenging, as they often occur gradually over large geographical areas. Here, we take advantage of a climatic transition zone, where cool‐affinity (kelp) and warm‐affinity (Sargassum) seaweed forests occur adjacently under similar environmental conditions, to test whether these seaweed habitats support different associated seaweed, invertebrate, coral, and fish assemblages. We found clear differences in associated seaweed assemblages between habitats characterized by kelp and Sargassum abundance, with kelp having higher biomass and seaweed diversity and more cool‐affinity species than Sargassum habitats. The multivariate invertebrate and fish assemblages were not different between habitats, despite a higher diversity of fish species in the Sargassum habitat. No pattern in temperature affinity of the invertebrate or fish assemblages in each habitat was found, and few fish species were exclusive to one habitat or the other. These findings suggest that, as ocean warming continues to replace kelps with Sargassum, the abundance and diversity of associated seaweeds could decrease, whereas fish could increase. Nevertheless, the more tropicalized seaweed habitats may provide a degree of functional redundancy to associated fauna in temperate seaweed habitats.
Genetic diversity can influence resilience and adaptative capacity of organisms to environmental change. Genetic diversity within populations is largely structured by reproduction, with the prevalence of asexual versus sexual reproduction often underpinning important diversity metrics that determine selection efficacy. Asexual or clonal reproduction is expected to reduce genotypic diversity and slow down adaptation through reduced selection efficacy, yet the evolutionary consequences of clonal reproduction remain unclear for many natural populations. Here, we examine the genomic consequences of sympatric sexual (haplodiplontic) and clonal morphs of the kelp Ecklonia radiata that occur interspersed on reefs in Hamelin Bay, Western Australia. Using genome-wide single nucleotide polymorphisms, we confirm significant asexual reproduction for the clonal populations, indicated by a significantly lower number of multi-locus lineages and higher intra-individual diversity patterns (individual multi-locus heterozygosity, MLH). Nevertheless, co-ancestry analysis and breeding experiments confirmed that sexual reproduction by the clonal morph and interbreeding between the two morphs is still possible, but varies among populations. One clonal population with long-term asexuality showed trends of decreased selection efficacy (increased ratio non- vs. synonymous gene diversities). Yet, all clonal populations showed distinct patterns of putative local adaptation relative to the sexual morph, possibly indicating maladaptation to local environmental conditions and high vulnerability of this unique clonal morph to environmental stress.
Marine heatwaves (MHWs) have caused declines in many kelp forests globally. Although the ecological effects of these climatic extremes have been well examined, studies on the role of genotypic variation in underpinning population responses under pressures are lacking. Understanding how kelps respond to different warming profiles and, in particular, intraspecific variation in responses is necessary to confidently anticipate the future of kelp forests, yet this remains a critical knowledge gap for most species. This study examined the responses of early life stages of 9 different genotypes of the Australian kelp Ecklonia radiata to different MHW profiles, where cumulative heat intensity was kept constant: control treatment (constant 19°C), heat spikes (fluctuating 19-23°C), low intensity MHW (ramp up 23°C) and high intensity MHW (ramp up 27°C). Overall, we found significant declines in E. radiata gametophyte performance in all MHW treatments and delays in sporophyte recruitment during MHW exposure. We also found significant genotype by environment (G×E) interactions, suggesting tolerance to acute thermal stress is influenced by genetic variation. Our results showed that offspring from different genotypes within the same population respond differently to MHWs, indicating that some genotypes are susceptible to MHWs while others are more resistant. While the effects on standing genetic variation and subsequent susceptibility to other stressors are unknown, our findings suggest that in addition to immediate impacts on marine organisms, natural genotypic variation in response to thermal anomalies may facilitate the gradual evolution of populations with increased thermal tolerance under future climates.
Climate change is increasingly impacting ecosystems globally. Understanding adaptive genetic diversity and whether it will keep pace with projected climatic change is necessary to assess species’ vulnerability and design efficient mitigation strategies such as assisted adaptation. Kelp forests are the foundations of temperate reefs globally but are declining in many regions due to climate stress. A lack of knowledge of kelp's adaptive genetic diversity hinders assessment of vulnerability under extant and future climates. Using 4245 single nucleotide polymorphisms (SNPs), we characterized patterns of neutral and putative adaptive genetic diversity for the dominant kelp in the southern hemisphere (Ecklonia radiata) from ~1000 km of coastline off Western Australia. Strong population structure and isolation‐by‐distance was underpinned by significant signatures of selection related to temperature and light. Gradient forest analysis of temperature‐linked SNPs under selection revealed a strong association with mean annual temperature range, suggesting adaptation to local thermal environments. Critically, modelling revealed that predicted climate‐mediated temperature changes will probably result in high genomic vulnerability via a mismatch between current and future predicted genotype–environment relationships such that kelp forests off Western Australia will need to significantly adapt to keep pace with projected climate change. Proactive management techniques such as assisted adaptation to boost resilience may be required to secure the future of these kelp forests and the immense ecological and economic values they support.
Here, we report for the first time the presence of Dictyota cyanoloma in southern California. Dictyota cyanoloma is conspicuous in harbors and bays by its distinctive bright blue‐iridescent margins. This species was originally described from Europe, but subsequent studies have revealed that it represented an introduction from Australia. The current distribution of D. cyanoloma comprises southern Australia and the North East Atlantic, including the Mediterranean Sea and the Macaronesian islands. The presence of D. cyanoloma in southern California is supported by molecular cox1 and psbA gene sequences. A reconstruction of the invasive history based on nine polymorphic microsatellite markers reveals a close affinity of the Californian specimens with European populations. Dictyota cyanoloma in the United States appears to be (so far) restricted to the Californian coast from San Diego Bay in the south to Santa Catalina Island and Long Beach Harbor in the north. A correlative species distribution model suggests gradually declining habitat suitability north of the Southern Californian Bight and high suitability in Baja California, including the Gulf of California. Finally, its widespread abundance in bays and harbors suggests shipping is a likely transport mechanism.
Extreme events are increasing globally with devastating ecological consequences, but the impacts on underlying genetic diversity and structure are often cryptic and poorly understood, hindering assessment of adaptive capacity and ecosystem vulnerability to future change. Using very rare "before" data we empirically demonstrate that an extreme marine heatwave caused a significant poleward shift in genetic clusters of kelp forests whereby alleles characteristic of cool water were replaced by those that predominated in warm water across 200 km of coastline. This "genetic tropicalisation" was facilitated by significant mortality of kelp and other co-occurring seaweeds within the footprint of the heatwave that opened space for rapid local proliferation of surviving kelp genotypes or dispersal and recruitment of spores from warmer waters. Genetic diversity declined and inbreeding increased in the newly tropicalised site, but these metrics were relative stable elsewhere within the footprint of the heatwave. Thus, extreme events such as marine heatwaves not only lead to significant mortality and population loss but can also drive significant genetic change in natural populations.
Aquaculture and maritime traffic have been identified as the main vectors for introductions of alien marine species. Except for one notorious case of Caulerpa taxifolia, the role of aquarium trade towards the introduction of alien seaweeds has been largely unassessed. Here, we address the risk of accidental release of seaweed species from the aquarium trade market in European waters. We assessed the importance and diversity of seaweed species in the European online aquarium retail circuit. Our web survey revealed more than 30 genera available for online sale into Europe, including known introduced and invasive species. A second aspect of the study consisted in sampling algal diversity found in aquaria. While allowing direct and accurate identification of the specimens, this approach was targeting not only ornamental species, but also seaweeds that may be accidentally present in the aquarium circuit. By DNA-barcoding we identified no less than 134 taxa, 7 of which are flagged as introduced in Europe and 5 reported as invasive. Climate envelope models show that at least 23 aquarium species have the potential to thrive in European waters. As expected by the tropical conditions in most aquaria, southern Atlantic regions of Europe and the Mediterranean are the most vulnerable towards new introductions. Further predictions show that this risk will increase and shift northwards as global warming proceeds. Overall our data indicate that aquarium trade poses a potential risk of new seaweed introductions, and calls for a cautious approach.
The World Register of Marine Species (WoRMS) celebrated its 10th anniversary in 2017. WoRMS is a unique database: there is no comparable global database for marine species, which is driven by a large, global expert community, is supported by a Data Management Team and can rely on a permanent host institute, dedicated to keeping WoRMS online. Over the past ten years, the content of WoRMS has grown steadily, and the system currently contains more than 242,000 accepted marine species. WoRMS has not yet reached completeness: approximately 2,000 newly described species per year are added, and editors also enter the remaining missing older names-both accepted and unaccepted-an effort amounting to approximately 20,000 taxon name additions per year. WoRMS is used extensively, through different channels, indicating that it is recognized as a high-quality database on marine species information. It is updated on a daily basis by its Editorial Board, which currently consists of 490 taxonomic and thematic experts located around the world. Owing to its unique qualities, WoRMS has become a partner in many large-scale initiatives including OBIS, LifeWatch and the Catalogue of Life, where it is recognized as a high-quality and reliable source of information for marine taxonomy.