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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., (© 2023 The Authors. Journal of Phycology published by Wiley Periodicals LLC on behalf of Phycological Society of America.)

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., (© The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

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., (© 2022 John Wiley & Sons Ltd.)

Single-gene markers, such as the mitochondrial cox1, microsatellites, and single-nucleotide polymorphisms are powerful methods to describe diversity within and among taxonomic groups and characterize phylogeographic patterns. Large repositories of publicly-available, molecular data can be combined to generate and evaluate evolutionary hypotheses for many species, including algae. In the case of biological invasions, the combination of different molecular markers has enabled the description of the geographic distribution of invasive lineages. Here, we review the phylogeography of the widespread invasive red macroalga Agarophyton vermiculophyllum (synonym Gracilaria vermiculophylla). The cox1 barcoding provided the first description of the invasion history and hinted at a strong genetic bottleneck during the invasion. Yet, more recent microsatellite and SNP genotyping has not found evidence for bottlenecks and instead suggested that genetically diverse inocula arose from a highly diverse source population, multiple invasions, or some mix of these processes. The bottleneck evident from cox1 barcoding likely reflects the dominance of one mitochondrial lineage, and one haplotype in particular, in the northern source populations in Japan. Recent cox1 sequencing of A. vermiculophyllum has illuminated the complexity of phylogeographic structure in its native range of the northwest Pacific Ocean. For example, the western coast of Honshu in the Sea of Japan displays spatial patterns of haplotypic diversity with multiple lineages found together at the same geographic site. By consolidating the genetic data of this species, we clarify the phylogenetic relationships of a well-studied macroalga introduced to virtually every temperate estuary of the Northern Hemisphere., (© 2021 Phycological Society of America.)

Invasive species are co-introduced with microbiota from their native range and also interact with microbiota found in the novel environment to which they are introduced. Host flexibility toward microbiota, or host promiscuity, is an important trait underlying terrestrial plant invasions. To test whether host promiscuity may be important in macroalgal invasions, we experimentally simulated an invasion in a common garden setting, using the widespread invasive macroalga Agarophyton vermiculophyllum as a model invasive seaweed holobiont. After disturbing the microbiota of individuals from native and non-native populations with antibiotics, we monitored the microbial succession trajectories in the presence of a new source of microbes. Microbial communities were strongly impacted by the treatment and changed compositionally and in terms of diversity but recovered functionally by the end of the experiment in most respects. Beta-diversity in disturbed holobionts strongly decreased, indicating that different populations configure more similar -or more common- microbial communities when exposed to the same conditions. This decline in beta-diversity occurred not only more rapidly, but was also more pronounced in non-native populations, while individuals from native populations retained communities more similar to those observed in the field. This study demonstrates that microbial communities of non-native A. vermiculophyllum are more flexibly adjusted to the environment and suggests that an intraspecific increase in host promiscuity has promoted the invasion process of A. vermiculophyllum. This phenomenon may be important among invasive macroalgal holobionts in general.

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., (© 2020 Phycological Society of America.)

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., (© 2020 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

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]

Determining the relative importance of sexual and asexual reproduction is critical for determining how genetic diversity is partitioned within and among populations. Macroalgae exhibit reproductive system variability, with many species capable of both sexual and asexual reproduction. Thus, rates of fragmentation (asexual) versus sporic recruitment (sexual) must be quantified. This is critical during range expansions when shifts to uniparental reproduction are common. Chondria tumulosa is a cryptogenic red alga that was discovered forming thick mats at Manawai, in the Northwestern Hawaiian Islands, during opportunistic sampling in 2019. It reduced the biodiversity and abundance of associated coral reef organisms. To characterize the reproductive system of C. tumulosa in this atoll, we visually assessed 124 thallus clumps for reproductive structures and used five microsatellite loci to genotype 41 thalli. All thalli bearing reproductive structures (20%) and all thalli that were genotyped were tetrasporophytes. No gametophytic thalli were observed using microscopy or microsatellite genotyping, though 80% of thalli observed under the microscope were vegetative. We observed in situ thallus fragmentation supported by the presence of 17 repeated genotypes and other genetic signatures, suggesting high rates of asexual reproduction. These results suggest that C. tumulosa is partially clonal in this atoll and has the potential for spreading to other nearby atolls. Rapid establishment, thallus fragmentation and tetrasporophytic dominance are consistent with other red macroalgal invasions studied to date. Understanding the reproductive system is an important component of developing management strategies for this alga and expanding our understanding of the population genetics of partially clonal taxa. [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]

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 rapid evolution of non-native species can facilitate invasion success, but recent reviews indicate that such microevolution rarely yields expansion of the climatic niche in the introduced habitats. However, because some invasions originate from a geographically restricted portion of the native species range and its climatic niche, it is possible that the frequency, direction, and magnitude of phenotypic evolution during invasion have been underestimated. We explored the utility of niche shift analyses in the red seaweed Gracilaria vermiculophylla, which expanded its range from the northeastern coastline of Japan to North America, Europe, and northwestern Africa within the last 100 years. A genetically informed climatic niche shift analysis indicates that native source populations occur in colder and highly seasonal habitats, while most non-native populations typically occur in warmer, less seasonal habitats. This climatic niche expansion predicts that non-native populations evolved greater tolerance for elevated heat conditions relative to native source populations. We assayed 935 field-collected and 325 common-garden thalli from 40 locations, and as predicted, non-native populations had greater tolerance for ecologically relevant extreme heat (40°C) than did Japanese source populations. Non-native populations also had greater tolerance for cold and low-salinity stresses relative to source populations. The importance of local adaptation to warm temperatures during invasion was reinforced by evolution of parallel clines: Populations from warmer, lower-latitude estuaries had greater heat tolerance than did populations from colder, higher-latitude estuaries in both Japan and eastern North America. We conclude that rapid evolution plays an important role in facilitating the invasion success of this and perhaps other non-native marine species. Genetically informed ecological niche analyses readily generate clear predictions of phenotypic shifts during invasions and may help to resolve debate over the frequency of niche conservatism versus rapid adaptation during invasion. [ABSTRACT FROM AUTHOR]

Haploid-diploid life cycles impose unique eco-evolutionary consequences, rendering commonly used proxies difficult to use (e.g. separate sexes prevent selfing). Population genetic analyses are therefore required to explore patterns of reproductive system variation. However, there are still few haploiddiploid species for which polymorphic, nuclear loci exist. This problem is particularly acute for algae. Here, we describe the development of the first microsatellite loci in a freshwater red alga. We tested 73 candidate loci against a panel of Batrachospermum gelatinosum (L.) De Candolle gametophytes that encompass much of its North American range. Ten loci consistently amplified and were characterized by clean peak architectures on a capillary sequencer with one allele per locus, as expected in a haploid gametophyte. We then explored some basic population genetic indices in gametophytes collected from one site and obtained good resolution based on the probability of identity (pid). Yet, we observed a pattern of clumped repeated genotypes throughout the stream reach sampled. The pattern of moderate genotypic richness could be due to intragametophytic selfing resulting in the complete loss of genetic diversity from a single gamete union. Future studies will need to sample more populations to determine if intragametophytic selfing is the dominant reproductive mode in this monoicous taxon. The loci developed here represent an important tool for studying freshwater red algal populations in specific as well as enhancing our understanding of reproductive system variation and the haploid-diploid life cycle of algae in general. [ABSTRACT FROM AUTHOR]

Chondrus crispus, or Irish moss, is a common edible red seaweed that can be found on rocky shores in the Northern Atlantic. The cell wall contains carrageenan and C. crispus is the original source of this commercially used thickener. Because of the ecological and economic importance of this red alga a relatively important research literature exists and one of the recent achievements in C. crispus research is the sequencing of its genome. In this chapter we review some of the literature with the aim to promote C. crispus as a model organism for florideophyte red seaweeds. We consider subjects like commercial and historical uses, ecology, genetics, population structure, mating systems, physiology, cell wall biology and genomics. [ABSTRACT FROM AUTHOR]