These fish are full of surprises

Deep-sea anglerfishes are not only incredibly ugly, with bizarre ways of reproducing and luring prey; they have now sent scientists into a spin with seemingly law-defying immune adaptations that could have implications for humans.

It’s to do with the way tiny males permanently attach themselves to larger females, fusing tissues and blood circulation to feed off their mate’s nutrient intake and supply sperm – a unique phenomenon discovered 100 years ago, known as sexual parasitism.

In vertebrates, this tissue fusing shouldn’t be possible, says Thomas Boehm from Germany’s Max Planck Institute, as the immune system would ordinarily rally to the defence.

“Sexual parasitism represents a form of anatomical joining that puzzles any immunologist, he says. “How can two individuals seamlessly fuse their bodies when tissue rejection and destruction is the norm when we attempt organ transplantation?”

Boehm is senior author of a study published in the journal Science that used genome sequencing of anglerfish (Lophiiformes) and analysis of genes known to play roles in immunity to try and unravel the mystery.

Working around the challenge of sourcing specimens, Boehm and colleagues, including Theodore Pietsch from the University of Washington, US, and first author Jeremy Swann, ground up frozen tissue and sequenced DNA from 31 preserved specimens from 10 species with various degrees of attachment, and from another 10 species that don’t attach.

They found “[s]triking modifications to immune facilities” depending on the permanency of the attachment, with a progressive loss of adaptive immunity. The mildest change, in more temporary attachments, was a lack of critical genes that underpin mature antibody responses.

In the most drastic adaptation, they were astonished to find a loss of antibodies and killer T cell functions altogether. “This was considered impossible for vertebrates to achieve by everybody, including myself,” says Boehm.

If humans lose these genes, they are severely ill and can’t live for long without a bone marrow transplant to supply a new immune system. To survive without this immune defence is thus quite extraordinary, according to Boehm.

For hundreds of millions of years, innate and adaptive immunity have co-evolved and were thought to be indispensable for survival.

Innate immunity refers to the body’s inborn, non-specific immune mechanisms that provide a first line of defence against foreign invaders.

Adaptive, or acquired, immunity involves antibodies that target specific pathogens after exposure to them, and is unique to vertebrates. It develops over time, providing lifelong immunity via highly specialised T cells.

Anglerfishes, the deep-sea’s most species-rich vertebrate group, seem to have worked around this system in pursuit of reproductive success, which the authors suggest could have been driven by a restructuring of their innate immune defences.

Given that vertebrates “inhabit a vast variety of ecological niches, from the deep sea to the high altitudes of the Andes,” Boehm says it follows that their immune systems would adapt to their unique habitats, something that has been underexplored by immunologists.

“Our study shows that it is possible, for some species at least, to disentangle a co-evolutionary cooperation that lasted 400 million years and to survive on innate immunity alone,” he adds.

“So nature is very ingenious, and we may be able to learn from this on how to increase innate immune facilities in patients whose adaptive immune system fails. Something for the future, but clearly worth pursuing.”