Coevolution of the Tlx homeobox gene with medusa development (Cnidaria: Medusozoa)

Cnidarians display a wide diversity of life cycles. Among the main cnidarian clades, only Medusozoa possesses a swimming life cycle stage called the medusa, alternating with a benthic polyp stage. The medusa stage was repeatedly lost during medusozoan evolution, notably in the most diverse medusozoan class, Hydrozoa. Here, we show that the presence of the homeobox gene Tlx in Cnidaria is correlated with the presence of the medusa stage, the gene having been lost in clades that ancestrally lack a medusa (anthozoans, endocnidozoans) and in medusozoans that secondarily lost the medusa stage. Our characterization of Tlx expression indicate an upregulation of Tlx during medusa development in three distantly related medusozoans, and spatially restricted expression patterns in developing medusae in two distantly related species, the hydrozoan Podocoryna carnea and the scyphozoan Pelagia noctiluca. These results suggest that Tlx plays a key role in medusa development and that the loss of this gene is likely linked to the repeated loss of the medusa life cycle stage in the evolution of Hydrozoa. Analysis of the homeobox gene Tlx across cnidarian genomes highlights the presence of Tlx only in clades featuring the medusa life cycle stage, linking the loss of the gene to loss of the medusa in Hydrozoa evolution.

Automated summary

Cnidarians have diverse life cycles, and only Medusozoa has a swimming stage called the medusa, alternating with a benthic polyp stage. The presence of the homeobox gene Tlx in Cnidaria is correlated with the presence of the medusa stage, and its loss is linked to the repeated loss of medusa in Hydrozoa evolution. Tlx plays a key role in medusa development, and its expression patterns support this role.