In temperate coastal waters around the globe, waves crash against rocky coves and shallow tide pools. A frequent inhabitant of these turbulent waters is the brown alga Scytosiphon, a complex multicellular seaweed with differentiated cell types in its tissues and an intricate network of rootlike filaments that let it hold tight to solid surfaces. For most ecologists, the sight of Scytosiphon on the shore is nothing surprising—the species is but one of thousands of species of algae that typically variously populate the Earth’s water. But for the international team of collaborators behind a new paper in Nature Ecology & Evolution, the populations of Scytosiphon off Japan’s coast formed the basis for a new insight into the evolutionary underpinnings of reproduction.
This population of Scytosiphon, also known as “Amazon” algae, reproduces entirely through asexual reproduction, creating a one hundred percent female population. This might come as a surprise, given that the majority of plant and animal species reproduce sexually. For centuries, scientists have been aware of the curious minority of asexual eukaryotes. Evidence shows that all asexual eukaryotes can trace their evolutionary lineage to sexual ancestors, meaning that at some point, a switch had to take place.
The group behind the new study hoped to decipher what prompted the move from sexual to asexual reproduction. One way to answer this question involves examining molecular mechanisms and phylogenetics—the evolutionary history of life and the relationships between organisms. In their analysis, researchers from the Max Planck Institute for Biology Tübingen and Kobe University investigated the Amazons as model organisms. By comparing Amazon species to their closest sexual relatives, they hoped to understand the mechanisms explaining the emergence of asexuality.
“[The] transition to asexuality has been intensively studied in animals and land plants, but rarely in seaweeds,” said Masakazu Hoshino, lead author on the Scytosiphon study. “Although brown algae are phylogenetically distinct from animals and have entirely different life cycles, I find it interesting that we observed similarities in the transition to asexuality across such diverse organisms.”
It is commonly believed that asexual reproduction forms at “evolutionary dead ends,” meaning that asexual reproduction does not prompt future adaptations or genetic diversity in a species. Sexual relatives are assumed to have a higher fitness. However, research from the past decade out of the University of Lausanne, Switzerland, found empirical data showing that asexual insect populations had unexpectedly similar diversity and rates of adaptation as their sexual relatives. Therefore, it is still unclear whether transitions to asexuality consistently bring predicted genomic changes.
“Asexual organisms should have [an] advantage against biparental sexual organisms in the short time scale,” Hoshino said. “In theory, the intrinsic rate of increase of asexuals should be double that of biparental sexuals per generation. It is well known that asexual organisms have a broader distributional range compared with their closest sexuals.”
As evolutionary time progresses, it is feasible that more species will transition to reproducing asexually, but it is not guaranteed whether those asexual species will last. “The Amazon population we observed may also go extinct within tens of thousands of years, while sexual populations might still persist,” Hoshino said.
Beyond improving our understanding of asexual reproduction, the importance of this research stems from seaweed’s pivotal role in ecology. Seaweed can be compared to the trees of the sea, as they provide the basis for life in coastal areas. Hence, their survival is imperative for the health of the local ecosystem at large. The fact that this particular species switched reproductive patterns highlights how adaptable seaweeds are.
When it comes to what prompted the switch, the researchers had a few ideas. Since males are less tolerant to changes in environmental conditions, water temperature variations may have caused males to die off. The study also found data supporting another reason: parthenogenesis.
In standard sexual reproduction, most brown species are so-called broadcast spawners. Both male and female gametes disperse into the seawater, with the male gametes attracted to the females thanks to a unique pheromone. The gametes then fuse to form a zygote and, ultimately, an offspring. But female gametes, if alone in the seawater, can also produce their own offspring through parthenogenesis, a reproductive pathway that does not involve male gametes. Parthenogenesis, roughly translating to virgin origin, describes when female gametes grow into adult females that are identical to the single parent. Therefore, asexual reproduction can proceed in the presence of a smaller percentage of males.
This cycle promotes increased numbers of female offspring and a decreased reliance on males, prompting the females to “defeminize” over generations. If the females no longer need to attract a male, certain traits such as the female pheromone become obsolete. The current generation of the Amazons has lost these pheromones and manages to produce relatively large gametes. Without the need for sexual partners, gender norms and the development of “attractive” female traits become redundant.
This pattern of defeminization matches the asexual transitions of other species, such as stick insects. Rather than a change in the male side, asexual reproduction is spurred more so by the loss of “female” functions. A unique aspect of the alga discovery is that this is one of the first recorded instances of the defeminization pattern occurring in a species with a haplodiplontic life cycle, meaning that the algae go through reproductive phases with spores and gametes.
Though similar research has been performed before, this study came with unique questions. Namely, researchers were puzzled by the process by which the gametes recognize each other and fuse, which is distinct in every species. In broadcast spawning, it is imperative that the male gametes recognize and fuse with female gametes. This complicated search process is controlled by gamete recognition genes (GRGs), which encode for features that allow potential partners to distinguish between each gender’s gametes.
“I often observed gametic incompatibilities acting as reproductive barriers among Scytosiphon species,” Hoshino said. “However, in brown algae, GRGs have yet to be identified.” Typically, GRGs are found by examining mutants with abnormalities in their fertilization capacities. However, Hoshino took a different approach: he examined and contrasted the parthenogenetic females to their sexual counterparts.
Hoshino discovered that multiple Amazon asexual lineages had several repressed genes. If that was the only difference, the GRGs could be deduced, but the issue was that the lineages had too many dissimilar genes, making it difficult to pinpoint which genes served as GRGs. “Moving forward, I expect to explore the function of genes with convergent expression shifts or those with parthenogenetic female-specific nonsynonymous mutations in greater detail,” Hoshino said. In other words, he hopes to narrow down which dissimilar genes play an active role in gamete attraction. This future work will enhance the understanding of gendered gene function in asexual reproduction.
As a veritable seaweed guru, Hoshino is excited to continue unraveling the mysteries behind seaweed reproduction. Dating back to his undergraduate career, Hoshino has been interested in studying seaweed, with a focus on taxonomy. “I was deeply impressed by the diversity of seaweeds in terms of shape, color, life cycle, and so on,” Hoshino said. This curiosity initially led Hoshino to study brown algae, which is how he stumbled upon the all-female population of the Amazons in Japan.
Across the Japanese shore and around the world, thousands of seaweed populations have yet to be explored. With their diversity of adaptations and variations, they hold the potential to catalyze new discoveries that will advance our understanding of biology and asexual reproduction.