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The relative frequency of sexual versus asexual reproduction governs the distribution of genetic diversity within and among populations. Most studies on the consequences of reproductive variation focus on the mating system (i.e., selfing vs. outcrossing) of diploid‐dominant taxa (e.g., angiosperms), often ignoring asexual reproduction. Although reproductive systems are hypothesized to be correlated with life‐cycle types, variation in the relative rates of sexual and asexual reproduction remains poorly characterized across eukaryotes. This is particularly true among the three major lineages of macroalgae (green, brown, and red). The Rhodophyta are particularly interesting, as many taxa have complex haploid–diploid life cycles that influence genetic structure. Though most marine reds have separate sexes, we show that freshwater red macroalgae exhibit patterns of switching between monoicy and dioicy in sister taxa that rival those recently shown in brown macroalgae and in angiosperms. We advocate for the investigation of reproductive system evolution using freshwater reds, as this will expand the life‐cycle types for which these data exist, enabling comparative analyses broadly across eukaryotes. Unlike their marine cousins, species in the Batrachospermales have macroscopic gametophytes attached to filamentous, often microscopic sporophytes. While asexual reproduction through monospores may occur in all freshwater reds, the Compsopogonales are thought to be exclusively asexual. Understanding the evolutionary consequences of selfing and asexual reproduction will aid in our understanding of the evolutionary ecology of all algae and of eukaryotic evolution generally. [ABSTRACT FROM AUTHOR]

Summary: Rhodophyta (or red algae) are a diverse and species‐rich group that forms one of three major lineages in the Archaeplastida, a eukaryotic supergroup whose plastids arose from a single primary endosymbiosis. Red algae are united by several features, such as relatively small intron‐poor genomes and a lack of cytoskeletal structures associated with motility like flagella and centrioles, as well as a highly efficient photosynthetic capacity. Multicellular red algae (or macroalgae) are one of the earliest diverging eukaryotic lineages to have evolved complex multicellularity, yet despite their ecological, evolutionary, and commercial importance, they have remained a largely understudied group of organisms. Considering the increasing availability of red algal genome sequences, we present a broad overview of fundamental aspects of red macroalgal biology and posit on how this is expected to accelerate research in many domains of red algal biology in the coming years. [ABSTRACT FROM AUTHOR]

Meiosis and syngamy generate an alternation between two ploidy stages, but the timing of these two processes varies widely across taxa, thereby generating life cycle diversity. One hypothesis suggests that life cycles with long‐lived haploid stages are correlated with selfing, asexual reproduction, or both. Though mostly studied in angiosperms, selfing and asexual reproduction are often associated with marginal habitats. Yet, in haploid‐diploid macroalgae, these two reproductive modes have subtle but unique consequences whereby predictions from angiosperms may not apply. Along the western Antarctic Peninsula, there is a thriving macroalgal community, providing an opportunity to explore reproductive system variation in haploid‐diploid macroalgae at high latitudes where endemism is common. Plocamium sp. is a widespread and abundant red macroalga observed within this ecosystem. We sampled 12 sites during the 2017 and 2018 field seasons and used 10 microsatellite loci to describe the reproductive system. Overall genotypic richness and evenness were high, suggesting sexual reproduction. Eight sites were dominated by tetrasporophytes, but there was strong heterozygote deficiency, suggesting intergametophytic selfing. We observed slight differences in the prevailing reproductive mode among sites, possibly due to local conditions (e.g., disturbance) that may contribute to site‐specific variation. It remains to be determined whether high levels of selfing are characteristic of macroalgae more generally at high latitudes, due to the haploid‐diploid life cycle, or both. Further investigations of algal life cycles will likely reveal the processes underlying the maintenance of sexual reproduction more broadly across eukaryotes, but more studies of natural populations are required. [ABSTRACT FROM AUTHOR]

Macroalgal (seaweed) genomic resources are generally lacking as compared with other eukaryotic taxa, and this is particularly true in the red algae (Rhodophyta). Understanding red algal genomes is critical to understanding eukaryotic evolution given that red algal genes are spread across eukaryotic lineages from secondary endosymbiosis and red algae diverged early in the Archaeplastids. The Gracilariales is a highly diverse and widely distributed order including species that can serve as ecosystem engineers in intertidal habitats and several notorious introduced species. The genus Gracilaria is cultivated worldwide, in part for its production of agar and other bioactive compounds with downstream pharmaceutical and industrial applications. This genus is also emerging as a model for algal evolutionary ecology. Here, we report new whole-genome assemblies for two species (Gracilaria chilensis and Gracilaria gracilis), a draft genome assembly of Gracilaria caudata , and genome annotation of the previously published Gracilaria vermiculophylla genome. To facilitate accessibility and comparative analysis, we integrated these data in a newly created web-based portal dedicated to red algal genomics (https://rhodoexplorer.sb-roscoff.fr). These genomes will provide a resource for understanding algal biology and, more broadly, eukaryotic evolution. [ABSTRACT FROM AUTHOR]

Invasive species can successfully and rapidly colonize new niches and expand ranges via founder effects and enhanced tolerance towards environmental stresses. However, the underpinning molecular mechanisms (i.e., gene expression changes) facilitating rapid adaptation to harsh environments are still poorly understood. The red seaweed Gracilaria vermiculophylla, which is native to the northwest Pacific but invaded North American and European coastal habitats over the last 100 years, provides an excellent model to examine whether enhanced tolerance at the level of gene expression contributed to its invasion success. We collected G. vermiculophylla from its native range in Japan and from two non‐native regions along the Delmarva Peninsula (Eastern United States) and in Germany. Thalli were reared in a common garden for 4 months at which time we performed comparative transcriptome (mRNA) and microRNA (miRNA) sequencing. MRNA‐expression profiling identified 59 genes that were differently expressed between native and non‐native thalli. Of these genes, most were involved in metabolic pathways, including photosynthesis, abiotic stress, and biosynthesis of products and hormones in all four non‐native sites. MiRNA‐based target‐gene correlation analysis in native/non‐native pairs revealed that some target genes are positively or negatively regulated via epigenetic mechanisms. Importantly, these genes are mostly associated with metabolism and defence capability (e.g., metal transporter Nramp5, senescence‐associated protein, cell wall‐associated hydrolase, ycf68 protein and cytochrome P450‐like TBP). Thus, our gene expression results indicate that resource reallocation to metabolic processes is most likely a predominant mechanism contributing to the range‐wide persistence and adaptation of G. vermiculophylla in the invaded range. This study, therefore, provides molecular insight into the speed and nature of invasion‐mediated rapid adaption. [ABSTRACT FROM AUTHOR]

Seaweeds are colonized by a microbial community, which can be directly linked to their performance. This community is shaped by an interplay of stochastic and deterministic processes, including mechanisms which the holobiont host deploys to manipulate its associated microbiota. The Anna Karenina principle predicts that when a holobiont is exposed to suboptimal or stressful conditions, these host mechanisms may be compromised. This leads to a relative increase of stochastic processes that may potentially result in the succession of a microbial community harmful to the host. Based on this principle, we used the variability in microbial communities (i.e., beta diversity) as a proxy for stability within the invasive holobiont Gracilaria vermiculophylla during a simulated invasion in a common garden experiment. Independent of host range, host performance declined at elevated temperature (22°C) and disease incidence and beta diversity increased. Under thermally stressful conditions, beta diversity increased more in epibiota from native populations, suggesting that epibiota from non‐native holobionts are thermally more stable. This pattern reflects an increase in deterministic processes acting on epibiota associated with non‐native hosts, which in the setting of a common garden can be assumed to originate from the host itself. Therefore, these experimental data suggest that the invasion process may have selected for hosts better able to maintain stable microbiota during stress. Future studies are needed to identify the underlying host mechanisms. [ABSTRACT FROM AUTHOR]

Fungal symbionts of terrestrial plants are among the most widespread and well‐studied symbioses, relatively little is known about fungi that are associated with macroalgae. To fill the gap in marine fungal taxonomy, we combined simple culture methods with amplicon sequencing to characterize the fungal communities associated with three brown (Sargassum muticum, Pelvetia canaliculata, and Himanthalia elongata) and two red (Mastocarpus stellatus and Chondrus crispus) macroalgae from one intertidal zone. In addition to characterizing novel fungal diversity, we tested three hypotheses: fungal diversity and community composition vary (i) among species distributed at different tidal heights, (ii) among tissue types (apices, mid‐thallus, and stipe), and (iii) among "isomorphic" C. crispus life cycle stages. Almost 70% of our reads were classified as Ascomycota, 29% as Basidiomycota, and 1% that could not be classified to a phylum. Thirty fungal isolates were obtained, 18 of which were also detected with amplicon sequencing. Fungal communities differed by host and tissue type. Interestingly, P. canaliculata, a fucoid at the extreme high intertidal, did not show differences in fungal diversity across the thallus. As found in filamentous algal endophytes, fungal diversity varied among the three life cycle stages in C. crispus. Female gametophytes were also compositionally more dispersed as compared to the fewer variable tetrasporophytes and male gametophytes. We demonstrate the utility of combining relatively simple cultivation and sequencing approaches to characterize and study macroalgal–fungal associations and highlight the need to understand the role of fungi in near‐shore marine ecosystems. [ABSTRACT FROM AUTHOR]

For many taxa, including isomorphic haplodiplontic macroalgae, determining sex and ploidy is challenging, thereby limiting the scope of some population demographic and genetic studies. Here, we used double‐digest restriction site‐associated DNA sequencing (ddRAD‐seq) to identify sex‐linked molecular markers in the widespread red alga Agarophyton vermiculophyllum. In the ddRAD‐seq library, we included 10 female gametophytes, 10 male gametophytes, and 16 tetrasporophytes from one native and one non‐native site (N = 40 gametophytes and N = 32 tetrasporophytes total). We identified seven putatively female‐linked and 19 putatively male‐linked sequences. Four female‐ and eight male‐linked markers amplified in all three life cycle stages. Using one female‐ and one male‐linked marker that were sex‐specific, we developed a duplex PCR and tested the efficacy of this assay on a subset of thalli sampled at two sites in the non‐native range. We confirmed ploidy based on the visual observation of reproductive structures and previous microsatellite genotyping at 10 polymorphic loci. For 32 vegetative thalli, we were able to assign sex and confirm ploidy in these previously genotyped thalli. These markers will be integral to ongoing studies of A. vermiculophyllum invasion. We discuss the utility of RAD‐seq over other approaches previously used, such as RAPDs (random amplified polymorphic DNA), for future work designing sex‐linked markers in other haplodiplontic macroalgae for which genomes are lacking. [ABSTRACT FROM AUTHOR]

Communities are shaped by scale dependent processes. To study the diversity and variation of microbial communities across scales, the invasive and widespread seaweed Agarophyton vermiculophyllum presents a unique opportunity. We characterized pro‐ and eukaryotic communities associated with this holobiont across its known distribution range, which stretches over the northern hemisphere. Our data reveal that community composition and diversity in the holobiont vary at local but also larger geographic scales. While processes acting at the local scale (i.e., within population) are the main structuring drivers of associated microbial communities, changes in community composition also depend on processes acting at larger geographic scales. Interestingly, the largest analysed scale (i.e., native and non‐native ranges) explained variation in the prevalence of predicted functional groups, which could suggest a functional shift in microbiota occurred over the course of the invasion process. While high variability in microbiota at the local scale supports A. vermiculophyllum to be a generalist host, we also identified a number of core taxa. These geographically independent holobiont members imply that cointroduction of specific microbiota may have additionally promoted the invasion process. [ABSTRACT FROM AUTHOR]

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self‐fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (FIS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in FIS within invertebrates is related to the potential to self‐fertilize, disperse, and choose mates. The similarity of FIS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and FIS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization. [ABSTRACT FROM AUTHOR]

Gracilaria vermiculophylla (Ohmi) Papenfuss, 1967 is a red alga native to the northwest Pacific, but over the last 100 years, this ecosystem engineer has invaded estuaries throughout the Northern Hemisphere. Despite previous studies documenting populations in estuarine habitats in British Columbia, California, and Baja California, our knowledge of its distribution along the North American Pacific is incomplete. In 2017, we surveyed 61 sites from Chusini Cove (Prince of Wales Island, Alaska) to Bayside Park (San Diego Bay, California), spanning more than 23… of latitude. We documented 33 new sites where G. vermiculophylla is currently found, but may have been previously overlooked, or not recognized. Many of these locations were areas of intensive shellfish aquaculture, particularly oysters, and are also important flyover stops for migrating birds, possibly contributing to the spread of this seaweed. Our study fills in the significant gaps in the distribution of G. vermiculophylla in North America, and, as such, will be an important contribution to future studies on the ecological and evolutionary consequences of this widespread marine invasion along this coastline. [ABSTRACT FROM AUTHOR]

The mating system partitions genetic diversity within and among populations and the links between life history traits and mating systems have been extensively studied in diploid organisms. As such most evolutionary theory is focused on species for which sexual reproduction occurs between diploid male and diploid female individuals. However, there are many multicellular organisms with biphasic life cycles in which the haploid stage is prolonged and undergoes substantial somatic development. In particular, biphasic life cycles are found across green, brown and red macroalgae. Yet, few studies have addressed the population structure and genetic diversity in both the haploid and diploid stages in these life cycles. We have developed some broad guidelines with which to develop population genetic studies of haploid-diploid macroalgae and to quantify the relationship between power and sampling strategy. We address three common goals for studying macroalgal population dynamics, including haploid-diploid ratios, genetic structure and paternity analyses. [ABSTRACT FROM AUTHOR]

Generalist consumers potentially limit introduced prey populations when they are willing and able to consume those prey, but because generalist consumers vary in feeding preference, they are not equally effective in resisting invasions. Previous work suggested that during the introduction of the red seaweed Gracilaria vermiculophylla to North American and European shorelines, populations evolved enhanced levels of constitutive and activated prostaglandin-based defenses against Littorina snails and the isopod Idotea balthica. However, when we offered tissue from a total of 700 G. vermiculophylla thalli from 14 native Japanese and 25 non-native sites to a North American population of the generalist amphipod Ampithoe valida, native and non-native populations were consumed at statistically indistinguishable rates. In contrast to previous results using Idotea and Littorina, we found no evidence that mechanical wounding of G. vermiculophylla altered palatability of thalli to A. valida. These results indicate either the strength of anti-herbivore defense varies across the geographic range in the seaweed’s native range in the Northwest Pacific, that the effectiveness of G. vermiculophylla to deter herbivores varies across generalist herbivore species, or both. In either case, we question the conclusion that rapid phenotypic shift in anti-herbivory traits to generalist herbivores occurred in this species. Future studies should focus on whether shifts in anti-herbivore defenses are adaptive by experimentally assessing species-specific herbivore impacts in native and non-native ranges. [ABSTRACT FROM AUTHOR]