Evolution of the vertebrate head is revealed by the rosette mesoderm

The vertebrate head comprises characteristic combinations of the cranium, brain, cranial nerves and head muscles. However, there have long been arguments about the developmental and evolutionary origins and the possible segmental nature of the head muscles, particularly those anterior to the otic vesicle. In gnathostomes, the presence of pre-otic segments (trunk somite homologs) has been denied by anti-segmentalists, but championed by segmentalists, who have focused on marginally detectable somitomeres or on more obvious head cavities. This metameric ideology has generated various definitions of segments, causing great controversy1,2, and the evaluation of such arguments has been impeded by the relative paucity of relevant work on the head mesoderm of cyclostomes (hagfishes and lampreys). Here, we demonstrate the presence of rosettes (which are reminiscent of somites) in the head mesoderm of lamprey (Lethenteron camtschaticum) embryos using confocal laser scanning and transmission electron microscopy. These transient rosettes, which were not segmented by acellular fissures and were genetically distinct from trunk somites, emerged several times during character individualization of the head muscles. This specialty of the rosette dynamics suggests that the lamprey head mesoderm evolved de novo, rather than from somites, and molecular comparison among deuterostomes supported this perspective.