Certain species of deep-sea anglerfish employ a unique reproduction strategy (sexual parasitism) that involves the permanent joining of males to females. Thomas Boehm and colleagues now report that these Ceratioidei fish have lost key components of adaptive immunity.

During mating, the tiny male deep-sea anglerfish attach themselves to relatively gigantic females. In some species, there is fusion of epidermal and dermal tissues and joining of circulatory systems, with the male becoming permanently dependent on the female for nutrients. Swann et al. set out to explore how this naturally occurring form of parabiosis can occur between non-identical individuals without provoking allogeneic rejection. They generated whole genome sequences for ten species of Ceratioidei that mate through temporary attachment (four species), permanent mono-attachment of one male and female (three species), or permanent multi-attachment of one female to more than one male (three species). As a control, they also generated genome sequences for three species of anglerfish that mate through non-attachment.

Credit: Theodore W. Pietsch, University of Washington

Comparing MHC gene loci, they found that non-attaching and temporarily attaching anglerfish possess a large number of U-type MHC class I genes (mhc1u), multiple mhc2a alleles and only a few Z-type MHC class I genes (mhc1z), which is typical of teleost fish. Although mhc2 diversity was maintained in anglerfish that show permanent mono-attachment, these fish showed loss of mhc1u genes and expansion of mhc1z genes. Notably, anglerfish that permanently attached to more than one mate had no functional mhc1u genes and at most only one or two mhc1z or mhc2a genes.

Analysis of genes encoding components of the adaptive immune system revealed more striking adaptations in Ceratioidei. The genes encoding CD8 were absent from the genomes of all six permanently attaching species, and the three species showing permanent multiple attachments were predicted to lack functional αβ T cell receptors. Of note, all ten attaching Ceratioidei species lacked the aicda gene, which is necessary for antibody affinity maturation, suggesting that attenuation of antibody responses may facilitate attachment. However, only two of the permanently multi-attaching species (Haplophryne mollis and Photocorynus spiniceps) showed a complete loss of antibody-mediated immunity. H. mollis and P. spiniceps also showed pseudogenization of rag1 and rag2, indicating that γδ T cells do not compensate for their loss of adaptive T cell and B cell responses.

the unique mating mode of these deep-sea anglerfish is associated with the loss of key components of the vertebrate adaptive immune system

Therefore, the unique mating mode of these deep-sea anglerfish is associated with the loss of key components of the vertebrate adaptive immune system. It will be fascinating to further study the unique immune systems of these fish and how they have evolved to protect against potential pathogens lurking in the deep sea.