The evolution of lamprey (Petromyzontida) life history and the origin of metamorphosis

Modern lampreys (Petromyzontiformes) are one of two lineages of surviving jawless fishes (agnathans), and are thus of critical importance to understanding the evolution of the vertebrates. Although their fossil record is meager, it appears they have remained morphologically conserved for at least 360 million years, but the origin of their multi-stage life history is unclear. Unlike hagfishes, the other extant group of jawless fishes, which exhibit direct development, all modern lampreys possess a complex life cycle which includes a long-lived freshwater larval (or ammocoete) period, followed by a true metamorphosis into a sexually-immature juvenile and then mature adult which differ dramatically in their morphology and ecology from the larva. Because of their basal position, it is critical to understand when the extant lamprey life history evolved, and if such a life history was present in the last common ancestor of agnathans and gnathostomes. Recent discoveries in paleontology, genomic analyses, and developmental biology are providing insights into this problem. The current review synthesizes these findings and concludes that the ancestral lamprey life cycle followed a direct development. We suggest that the larval period was short and relatively limited if present at all, but that the juvenile included modern larval traits; over the course of evolution, differential selection pressures throughout the lifetime produced distinct larval and juvenile/adult periods. Each period required the dramatically different morphologies seen in modern lampreys, ultimately requiring a true metamorphosis to accommodate the large changes in the body plan and to maximize the efficiency of each life period. As a result, modern lamprey life histories are a patchwork of ancestral and derived characters.