When attacked, hagfishes produce a soft, fibrous defensive slime within a fraction of a second by ejecting mucus and threads into seawater. The rapid setup and remarkable expansion of the slime make it a highly effective and unique form of defense. How this biomaterial evolved is unknown, although circumstantial evidence points to the epidermis as the origin of the thread- and mucus-producing cells in the slime glands. Here, we describe large intracellular threads within a putatively homologous cell type from hagfish epidermis. These epidermal threads averaged ~2 mm in length and ~0.5 μm in diameter. The entire hagfish body is covered by a dense layer of epidermal thread cells, with each square millimeter of skin storing a total of ~96 cm threads. Experimentally induced damage to a hagfish's skin caused the release of threads, which together with mucus, formed an adhesive epidermal slime that is more fibrous and less dilute than the defensive slime. Transcriptome analysis further suggests that epidermal threads are ancestral to the slime threads, with duplication and diversification of thread genes occurring in parallel with the evolution of slime glands. Our results support an epidermal origin of hagfish slime, which may have been driven by selection for stronger and more voluminous slime.
Keywords: biomaterial; cell biology; evolutionary biology; hagfish; morphogenesis; predator-prey interaction; transcriptomics.
Hagfishes are deep-sea animals, and they represent one of the oldest living relatives of animals with backbones. To defend themselves against predators, they produce a remarkable slime that is reinforced with fibers and can clog a predator’s gills, thwarting the attack. The slime deploys in less than half a second, exuding from specialized glands on the hagfish’s body and expanding up to 10,000 times its ejected volume. The defensive slime is highly dilute, consisting mostly of sea water, with low concentrations of mucus and strong, silk-like threads that are approximately 20 centimeters long. Where and how hagfish slime evolved remains a mystery. Zeng et al. set out to answer where on the hagfish’s body the slime glands originated, and how they may have evolved. First, Zeng et al. examined hagfishes and found that cells in the surface layer of their skin (the epidermis) produce threads roughly two millimeters in length that are released when the hagfish’s skin is damaged. These threads mix with the mucus that is produced by ruptured skin cells to form a slime that likely adheres to predators’ mouths. This slime could be a precursor of the slime produced by the specialized glands. To test this hypothesis, Zeng et al. analyzed which genes are turned on and off both in the hagfishes’ skin and in their slime glands. The patterns they found are consistent with the slime glands originating from the epidermis. Based on these results, Zeng et al. propose that ancient hagfishes first evolved the ability to produce slime with anti-predator effects when their skin was damaged in attacks. Over time, hagfishes that could produce and store more slime and eject it actively into a predator’s mouth likely had a better chance of surviving. This advantage may have led to the appearance of increasingly specialized glands that could carry out these functions. The findings of Zeng et al. will be of interest to evolutionary biologists, marine biologists, and those studying the ecology of predator-prey interactions. Because of its unique material properties, hagfish slime is also of interest to biophysicists, bioengineers and those engaged in biomimetic research. The origin of hagfish slime glands is an interesting example of how a new trait evolved, and may provide insight into the evolution of other adaptive traits.
© 2023, Zeng et al.