Evolution of a remarkable intracellular polymer and extreme cell allometry in hagfishes

• Published in: Current biology Vol. 31; no. 22; pp. 5062 - 5068.e4
• Main Authors: Zeng, Yu, Petrichko, Skylar, Nieders, Kristen, Plachetzki, David, Fudge, Douglas
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 22.11.2021
• Subjects: allometry; Animals; biofiber; body size; cell size; Hagfishes; Phylogeny; Polymers; predator-prey interaction; scaling; body size; allometry; scaling; biofiber; cell size; predator-prey interaction
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2021.08.066

The size of animal cells rarely scales with body size, likely due to biophysical and physiological constraints.1,2 In hagfishes, gland thread cells (GTCs) each produce a silk-like proteinaceous fiber called a slime thread.3,4 The slime threads impart strength to a hagfish’s defensive slime and thus are potentially subject to selection on their function outside of the body.5–8 Body size is of fundamental importance in predator-prey interactions, which led us to hypothesize that larger hagfishes produce longer and stronger slime threads than smaller ones.9 Here, by sampling a range of sizes of hagfish from 19 species, we systematically examined the scaling of GTC and slime-thread dimensions with body size within both phylogenetic and ontogenetic contexts. We found that the length of GTCs varied between 40 and 250 μm and scaled positively with body size, exhibiting an allometric exponent greater than those in other animal cells. Correspondingly, larger hagfishes produce longer and thicker slime threads and thus are equipped to defend against larger predators. With diameter and length varying 4-fold (0.7–4 μm and 5–22 cm, respectively) over a body-size range of 10–128 cm, the slime threads characterize the largest intracellular polymers known in biology. Our results suggest selection for stronger defensive slime in larger hagfishes has driven the evolution of extreme size and allometry of GTCs. [Display omitted] •Hagfish gland thread cells vary between 40 and 250 μm in length and 50-fold in volume•Larger gland thread cells are found in larger hagfishes and produce larger threads•Longer and thicker threads likely help defend against larger predators•Hagfish slime threads are by far the largest intracellular polymers known Animal cell size rarely changes with body size. Zeng et al. show that hagfish gland thread cells vary by 50-fold in volume as body length varies between 10 and 128 cm. Larger hagfishes have disproportionally larger gland thread cells to produce and store longer and thicker slime threads, which likely help defend against more powerful predators.