An atlas of anteriorhoxgene expression in the embryonic sea lamprey head:hox-code evolution in vertebrates

In the hindbrain and the adjacent cranial neural crest (NC) cells of jawed vertebrates (gnathostomes), nested and segmentally-restricted domains ofHoxgene expression provide a combinatorialHox-code for specifying regional properties during head development. Extant jawless vertebrates, such as the sea lamprey(Petromyzon marinus),can provide insights into the evolution and diversification of thisHox-code in vertebrates. There is evidence for gnathostome-like spatial patterns ofHoxexpression in lamprey; however, the expression domains of the majority of lampreyhoxgenes from paralogy groups (PG) 1-4 are yet to be characterized, so it is unknown whether they are coupled to hindbrain segments (rhombomeres) and NC. In this study, we systematically describe the spatiotemporal expression of all 14 sea lampreyhoxgenes from PG1-PG4 in the developing hindbrain and pharynx to investigate the extent to which their expression conforms to the archetypal gnathostome hindbrain and pharyngealhox-codes. We find many similarities inHoxexpression between lamprey and gnathostome species, particularly in rhombomeric domains during hindbrain segmentation and in the cranial neural crest, enabling inference of aspects ofHoxexpression in the ancestral vertebrate embryonic head. These data are consistent with the idea that aHoxregulatory network underlying hindbrain segmentation is a pan vertebrate trait. We also reveal differences in hindbrain domains at later stages, as well as expression in the endostyle and in pharyngeal arch (PA) 1 mesoderm. Our analysis suggests that manyHoxexpression domains that are observed in extant gnathostomes were present in ancestral vertebrates but have been partitioned differently acrossHoxclusters in gnathostome and cyclostome lineages after duplication.