Ancient origins sex chromosomes in brown algae

The genomes of brown algal species with diverse sexual systems reveal how sex chromosomes originate, evolve, and sometimes transform into autosomes

To the point

• Ancient origins of the U/V chromosomes: The sex chromosomes of brown algae originated between 450 and 224 million years ago. They carry a conserved set of sex-linked nuclear genes, including the crucial male-determining gene MIN. These have remained remarkably stable over vast evolutionary periods.
• Diverse structural evolution in the lineages: The sex chromosomes show lineage-specific diversification and rearrangement, with the acquisition of new genes associated with increased complexity in morphology and sexual dimorphism in different brown algae species.
• Dynamic sex determination systems: The study reveals the frequent evolution of “orphaned” or taxonomically restricted genes on sex chromosomes and demonstrates cases where the original U/V system has shifted radically or ceased to be a sex chromosome (known as an autosome), such as in two hermaphroditic species that acquired both sexual functions, and the emergence of a diploid sex determination system in Fucus serratus.
• Implications for understanding sex chromosome evolution: These findings challenge conventional views by showing that sex determination systems can be surprisingly dynamic. They can evolve, reinvent themselves, or collapse, highlighting brown algae as a powerful model for investigating fundamental aspects of sexual reproduction and chromosome evolution.

Sex determination is a cornerstone of biology, yet many mysteries remain about how sex chromosomes evolve, especially outside familiar mammal and bird systems. Unlike mammals, where sex is set at fertilisation by XX/XY chromosomes, brown algae determine sex during spore formation based on U (female) or V (male) sex chromosomes. Despite their importance, the rise, evolution, and demise of U/V sex chromosomes have remained an enigma.

This new research demonstrates that these specialised sex chromosomes arose between 450 and 224 million years ago. A key finding is the identification of a pivotal male-determining gene, MIN, as well as six other core sex-linked genes, which have astonishingly remained almost unchanged across these vast evolutionary timescales.

The study also reveals that the extent and gene content of the sex-determining region in these chromosomes have diversified uniquely across brown algal lineages, often expanding through chromosomal rearrangements and acquiring new, lineage-specific genes. These structural changes may be linked to the increasing morphological and reproductive complexity observed among different brown algal species.

The dynamic nature of sex determination systems

The study also highlights that “orphan” or taxonomically restricted genes (genes unique to certain lineages) evolve with unexpected frequency in U and V chromosomes, underscoring their dynamic nature. “The U/V sex chromosomes have unique genomic characteristics that make them prone to evolving orphan genes. This evolutionary pattern may provide important clues about how unique brown algal genes originated,” said Josué Barrera-Redondo, first author of the paper and former postdoctoral researcher at the Max Planck Institute for Biology Tübingen.

The international team, led by researchers from the Max Planck Institute for Biology Tübingen (Germany), in collaboration with the CNRS and the Genoscope (France), uncovered two surprising cases where the ancestral U/V sex chromosome system has radically changed or even disappeared, transforming into autosomes. In two hermaphroditic species, formerly male individuals acquired key female-specific genes, enabling them to develop the reproductive structures of both sexes. Meanwhile, the marine seaweed genus Fucus lost the U/V system when its lineage became completely diploid. The researchers found that new sex-determining genes supplanted the ancestral V chromosome gene MIN, marking a major shift in how sex is controlled genetically.

“Our research reveals that brown algal sex chromosomes manage a delicate balance between stability and surprising flexibility. This demonstrates how dynamic and diverse sex determination can be across the tree of life,” explains lead researcher Susana Coelho, Director of the Department of Algal Development and Evolution at the Max Planck Institute for Biology Tübingen.

These findings show how sex-determining systems can collapse and be replaced, demonstrating that even something as fundamental as “male” and “female” is not fixed forever. It highlights a dynamic evolutionary landscape where sex-determining systems can evolve in unexpected ways – how they originate, reinvent themselves to persevere, and sometimes transform into autosomes. This offers fresh insights into sexual reproduction as one of the most fundamental aspects of biology.

This comprehensive investigation into brown algal sex chromosomes increases our understanding of U/V chromosome evolution and positions brown algae as a powerful model to explore the genetic and evolutionary basis of sex determination.