Evolution of parental care and ovulation behavior in oysters.

Approximately half of all living oysters brood offspring in the inhalant chamber of their mantle cavities; the remainder are broadcast spawners which do not engage in parental care of young. Ostreid ovulation involves a complex behavioral sequence that results in the countercurrent passage of newly spawned eggs through the gills (ctenidia) and into the inhalant chamber. We constructed molecular and combined-evidence phylogenetic trees to test hypotheses concerning the directionality of parental care evolution, and the evolutionary significance of the trans-ctenidial ovulation pathway, in the Ostreidae. Representatives of all three ostreid subfamilies, together with gryphaeid and nonostreoidean pterioid outgroups, were sequenced for a 941-nucleotide fragment of the 28S ribosomal gene. Our phylogenetic analyses indicate that (1) the Ostreidae are robustly monophyletic, (2) broadcast spawning and larval planktotrophy are ancestral ostreid traits, (3) trans-ctenidial ovulation predates the evolution of parental care in ostreid lineages, and (4) brooding originated once in the common ancestor of the Ostreinae/Lophinae, involved a modification of the final behavioral step in the ancestral ovulation pathway, and has been retained in all descendent lineages. Our data permit an independent test of fossil-based ostreid phylogenetic hypotheses and provide novel insights into oyster evolution and systematics.