ABSTRACTThe evolution of vertebrates from an invertebrate chordate ancestor involved the evolution of new organs, tissues, and cell types. It was also marked by the origin and duplication of new gene families. If, and how, these morphological and genetic innovations are related is an unresolved question in vertebrate evolution. Hyaluronan is an extracellular matrix (ECM) polysaccharide important for water homeostasis and tissue structure. Vertebrates possess a novel family of hyaluronan binding proteins called Lecticans, and studies in jawed vertebrates (gnathostomes) have shown they function in many of the cells and tissues that are unique to vertebrates. This raises the possibility that the origin and/or expansion of this gene family helped drive the evolution of these vertebrate novelties. In order to better understand the evolution of thelecticangene family, and its role in the evolution of vertebrate morphological novelties, we investigated the phylogeny, genomic arrangement, and expression patterns of alllecticansin the sea lamprey (Petromyzon marinus), a jawless vertebrate. Though bothP. marinusand gnathostomes have fourlecticans, our phylogenetic and syntenic analyses suggest lampreylecticansare the result of one or more cyclostome-specific duplications. Despite the independent expansion of the lamprey and gnathostomelecticanfamilies, we find highly conserved expression oflecticansin vertebrate-specific and mesenchyme-derived tissues. We also find that, unlike gnathostomes, lamprey expresses itslecticanparalogs in distinct subpopulations of head skeleton precursors, potentially reflecting an ancestral diversity of skeletal tissue types. Together, these observations suggest that the ancestral pre-duplicationlecticanhad a complex expression pattern, functioned to support mesenchymal histology, and likely played a role in the evolution of vertebrate-specific cell and tissue types.
