Larval brooding damselfishes and shifting body proportions: does pelagic larval swimming constrain reef fish morphology?

The vast majority of reef fishes, including damselfishes, have a pelagic larval stage that ends when any surviving larvae swim to a reef to settle. An extremely rare alternative lifestyle is larval brooding, where both parents protect larvae on the reef for months until they disperse nearby. The monophyletic clade of larval brooders includes two genera Acanthochromis and Altrichthys. In examination of the skeletons of these damselfishes, we found that all species of damselfish that brood larvae on the reef have a uniquely increased precaudal vertebral count, while all typical damselfishes have an invariable vertebral count with a greater proportion of caudal vertebrae. To explore the significance of the vertebral differences, we measured body proportions of larval brooders vs relatives with the typical pelagic larval stage. We found increased body cavity area and reduced muscle area in the larval brooder Acanthochromis polyacanthus. Furthermore, populations of Acanthochromis throughout its range have evolved significantly different proportions. In a comparison of known larval swimming ability among reef fishes, the larval brooders performed most poorly. We propose that when larval brooding evolved, relaxed selection on larval swimming performance allowed a shift in body proportions to favor a larger body cavity and altered axial patterning. Enlarged body cavity gives a fitness advantage as females could hold more of the large eggs and increase clutch size.