Solenn Stoeckel’s research while affiliated with Institut Français de Recherche pour l'Exploitation de la Mer and other places

Reproductive modes, migration, genetic diversity and local adaptation are important evolutionary traits that limit species' ranges. Understanding the interactions between evolutionary and ecological processes at species' edges provides clues to how species adapt to rapid environmental changes. In the Arctic Ocean, melting sea ice and increasing human activity are bridging coastal populations that were once separated by extreme polar conditions. Aulactinia stella is a keystone tetraploid circumpolar sea anemone species that is witnessing these changes. Here, we investigated how reproduction and genetic diversity structured in A. stella populations and between adults and juveniles sampled across the Arctic Ocean. Outside Kamchatka, we only found females or individuals without gonads. Genetic indices and changes in genotype frequencies confirmed that this species reproduces partially by parthenogenesis. Populations on the Atlantic side were highly clonal, while those on the Pacific side reproduced more sexually. Allelic diversity was twice as high in Kamchatka and Kuril populations, suggesting North Pacific coasts being the main last glacial refugia of A. stella. Patterns of genetic differentiation between site pairs revealed gene flow routes extending from Kamchatka to Atlantic populations. These routes aligned with ocean currents and reduced sea ice, and not with the past maritime exchanges between Atlantic and Pacific Oceans. Within each population, only a subset of juvenile genetic diversity, mostly of local origin, was represented among established adults, suggesting local adaptation or kin recognition mechanisms promoting endemism. Juveniles showed less genetic differentiation across the Arctic Ocean, possibly indicating that global changes are favoring juvenile dispersal.

Sexual to asexual transition is described as a process whereby asexual lineages emerge within sexual species. This phenomenon gives rise to many questions about the maintenance of sexual reproduction and the evolution of asexuality in these organisms. The poplar rust fungus Melampsora larici-populina has a complex life cycle, which is typical of rust fungi (Pucciniales). It alternates between a sexual reproduction phase on larch trees (Larix spp.) and rounds of asexual multiplication on poplar trees (Populus spp.). This study challenges the classic understanding of the M. larici-populina life cycle. We conducted a comprehensive population genetic analysis, utilizing 21 microsatellite markers and data from 2,122 individuals gathered over an extended time from various locations in France. Our results demonstrate the existence of many distinct lineages that reproduce asexually through the years, skipping the sexual phase. A clustering analysis identified a group of multilocus lineages that displayed all hallmarks of the genetic consequences of asexual reproduction, including highly negative and large variance among loci of the inbreeding coefficient (FIS). This indirect evidence for asexual reproduction was confirmed by the direct observation of these asexual lineages being repeatedly sampled over the years. While sexual lineages are predominant throughout France, asexual lineages are more prevalent in the south of the country, due to possible environmental or ecological factors that allow the overwintering of asexual forms. The discovery of variations in the life cycle in this species offers insights into the evolution from sexual to asexual reproduction encountered in many pathogen species. It could serve as a model organism for studying the transition from sexual to asexual reproductive mode.

Temporal population genetic studies have investigated evolutionary processes, but few have characterized reproductive system variation. Yet, temporal sampling may improve our understanding of reproductive system evolution through the assessment of the relative rates of selfing, outcrossing, and clonality. In this study, we focused on the monoicous, haploid‐diploid freshwater red alga Batrachospermum gelatinosum . This species has a perennial, microscopic diploid phase (chantransia) that produces an ephemeral, macroscopic haploid phase (gametophyte). Recent work focusing on single‐time point genotyping suggested high rates of intragametophytic selfing, although there was variation among sites. We expand on this work by genotyping 191 gametophytes sampled from four sites that had reproductive system variation based on single‐snapshot genotyping. For this study, we sampled at multiple time points within and among years. Results from intra‐annual data suggested shifts in gametophytic genotypes throughout the season. We hypothesize that this pattern is likely due to the seasonality of the life cycle and the timing of meiosis among the chantransia. Interannual patterns were characterized by consistent genotypic and genetic composition, indicating stability in the prevailing reproductive system through time. Yet, our study identified limits by which available theoretical predictions and analytical tools can resolve reproductive system variation using haploid data. There is a need to develop new analytical tools to understand the evolution of sex by expanding our ability to characterize the spatiotemporal variation in reproductive systems across diverse life cycles.

Investigating taxa at varying stages of divergence can shed light on the evolutionary forces that lead to reproductive isolation and eventual speciation. The forces promoting isolation vary in space and time, which makes it difficult to reconstruct the trajectory that resulted in the divergence observed among species today. The red macroalgal genus Plocamium is known worldwide for its cryptic genetic and chemical diversity. Previous work on the genus Plocamium in Antarctica observed two haplotypes along the western Antarctic Peninsula that have been treated as the same species. Using 10 microsatellite loci, we observed that these two haplotypes correspond to two highly divergent, co‐occurring genetic entities in Antarctic Plocamium , which are located within close vicinity of each other at the same sites. The morphology of the reproductive structures, a feature commonly used to identify cryptic species in Plocamium , as well as the timing of reproduction, differed significantly between the two genetic entities. Altogether, this suggests that two Antarctic Plocamium species exist on the western Antarctic Peninsula. We observed evidence for high levels of selfing in both genetic entities, which likely exacerbated the lack of gene flow between them. In addition, we identified concomitant chemodiversity that generates compelling evidence of early evolutionary divergence within one of these entities. This chemodiversity has ecological consequences for its main grazer, which alludes to one putative evolutionary driver of divergence. Antarctic Plocamium spp. provide a promising model system for investigating the eco‐evolutionary forces that initiate and maintain species boundaries.

Life cycles with a prolonged haploid phase are thought to be correlated with greater rates of selfing and asexual reproduction. In red algae, recent population genetic studies have aimed to test this prediction but have mostly focused on marine species with separate sexes. We characterized the reproductive system of the obligately monoicous (i.e., hermaphroditic) freshwater red alga Batrachospermum gelatinosum and predicted that we would find genetic signatures of uniparental reproduction because of its haploid‐diploid life cycle. We sampled 18 sites and genotyped 311 gametophytes with 10 polymorphic microsatellite loci to describe the reproductive system. Genotypic richness was low (<0.5) and pareto β values (describing clonal membership) were <0.7 for most sites. In taxa with separate sexes, these patterns are typically indicative of asexual reproduction. However, the genetic consequences of selfing in monoicous gametophytes are indistinguishable from those caused by asexual processes. Since we sampled gametophytes and have not yet genotyped the chantransia (i.e., the diploid phase), we interpreted low diversity as a signature of intragametophytic selfing. Additionally, to understand the factors that drive selfing, we tested latitude and several other environmental variables, but none was significantly correlated with the genetic variation we observed. Nevertheless, future studies should genotype the chantransia to measure observed heterozygosity among other summary statistics to disentangle the effects of selfing versus asexual reproduction. Together, these data, coupled with further characterization of abiotic factors that influence population genetic patterns, will allow us to test potential drivers of reproductive system evolution.

The relative rates of sexual versus asexual reproduction influence the partitioning of genetic diversity within and among populations. During range expansions, asexual reproduction often facilitates colonization and establishment. The arrival of the green alga Avrainvillea lacerata has caused shifts in habitat structure and community assemblages since its discovery in 1981 offshore of Oʻahu, Hawai‘i. Field observations suggest this species is spreading via vegetative reproduction. To characterize the reproductive system of A. lacerata in Hawai‘i, we developed seven microsatellite loci and genotyped 321 blades collected between 2018 and 2023 from three intertidal sites at Maunalua Bay and ʻEwa Beach. We observed one to four alleles at multiple loci, suggesting A. lacerata is tetraploid. Each site was characterized by high genotypic richness ( R > 0.8). However, clonal rates were also high, suggesting the vegetative spread of A. lacerata plays a significant role. The importance of clonal reproduction for the persistence of A. lacerata in Hawai‘i is consistent with the ecological data collected for this species and observations of other abundant macroalgal invaders in Hawai‘i and other regions of the world. These data demonstrate the necessity for implementing appropriate population genetic methods and provide insights into the biology of this alga that will contribute to future studies on effective management strategies incorporating its reproductive system. This study represents one of the few that investigate green algal population genetic patterns and contributes to our understanding of algal reproductive system evolution.

Temporal population genetic studies have investigated evolutionary processes, but few have characterized the temporal patterns of reproductive system variation. Yet, temporal sampling may improve our understanding of reproductive system evolution through assessing the relative rates of selfing, outcrossing, and clonality. In this study, we focus on the monoicous, haploid-diploid freshwater red alga Batrachospermum gelatinosum. This species has a perennial, microscopic diploid phase (chantransia) that produces an ephemeral, macroscopic haploid phase (gametophyte). Recent work focusing on single time point genotyping suggested high rates of intragametophytic selfing, though there was variation among sites. We expand on this work by genotyping 191 gametophytes from four sites with reproductive system variation at multiple time points within and among years. Intra-annual data suggest shifts in gametophytic genotypes present throughout the gametophytic season. We hypothesize this pattern is likely due to the seasonality of the life cycle and the timing of meiosis among the chantransia. Inter-annual patterns were characterized by consistent genotypic and genetic composition, indicating stability in the prevailing reproductive system through time. Yet, our study identified limits to which available theoretical predictions and analytical tools can resolve reproductive system variation using haploid data. There is a need to develop better tools to understand the evolution of sex by expanding our ability to characterize the spatiotemporal variation in reproductive systems across diverse life cycles.

Pathogen species are experiencing strong joint demographic and selective events, especially when they adapt to a new host, for example through overcoming plant resistance. Stochasticity in the founding event and the associated demographic variations hinder our understanding of the expected evolutionary trajectories and the genetic structure emerging at both neutral and selected loci. What would be the typical genetic signatures of such a rapid adaptation event is not elucidated. Here, we build a demogenetic model to monitor pathogen population dynamics and genetic evolution on two host compartments (susceptible and resistant). We design our model to fit two plant pathogen life cycles, ‘with’ and ‘without’ host alternation. Our aim is to draw a typology of eco-evolutionary dynamics. Using time-series clustering, we identify three main scenarios: 1) small variations in the pathogen population size and small changes in genetic structure, 2) a strong founder event on the resistant host that in turn leads to the emergence of genetic structure on the susceptible host, and 3) evolutionary rescue that results in a strong founder event on the resistant host, preceded by a bot- tleneck on the susceptible host. We pinpoint differences between life cycles with notably more evolutionary rescue ‘with’ host alternation. Beyond the selective event itself, the demographic trajectory imposes specific changes in the genetic structure of the pathogen population. Most of these genetic changes are transient, with a signature of resistance overcoming that vanishes within a few years only. Considering time-series is therefore of utmost importance to accurately decipher pathogen evolution.

The relative rates of sexual versus asexual reproduction influence the partitioning of genetic diversity within and among populations. During range expansions, uniparental reproduction often facilitates colonization and establishment. The arrival of the green alga Avrainvillea lacerata has caused shifts in habitat structure and community assemblages since its discovery in 1981 offshore of west Oahu, Hawaii. Field observations suggest this species is spreading via vegetative reproduction. To characterize the reproductive system of A. lacerata in Hawaii, we developed seven microsatellite loci and genotyped 321 blades collected between 2018 and 2023 from two intertidal sites at Maunalua Bay and 'Ewa Beach. We found one to four alleles at multiple loci, suggesting A. lacerata is tetraploid. Each site was characterized by high genotypic richness (R > 0.8). However, clonal rates were also high at both sites, suggesting vegetative spread of A. lacerata plays a significant role. The importance of clonal reproduction for the persistence of A. lacerata in Hawaii is consistent with the ecological data collected for this species, and observations of other abundant macroalgal invaders in Hawaii and other regions of the world. These data demonstrate the necessity for implementing appropriate population genetic methods and provide insights into the biology of this alga that will contribute to future studies on effective management strategies incorporating its reproductive system. This study represents one of the few investigating green algal population genetic patterns and contributes to our understanding of algal reproductive system evolution.