Evolution of the Branchiostegal Membrane and Restricted Gill Openings in Actinopterygian Fishes

A phylogenetic survey is a powerful approach for investigating the evolutionary history of a morphological characteristic that has evolved numerous times without obvious functional implications. Restricted gill openings, an extreme modification of the branchioste- gal membrane, are an example of such a characteristic. We examine the evolution of branchiostegal membrane morphology and highlight convergent evolution of restricted gill openings. We surveyed specimens from 433 families of actinopterygians for branchiostegal membrane morphology and measured head and body dimensions. We inferred a relaxed molecular clock phylogeny with branch length estimates based on nine nuclear genes sampled from 285 species that include all major lineages of Actinopterygii. We calculated marginal state reconstruc- tions of four branchiostegal membrane conditions and found that restricted gill openings have evolved independ- ently in at least 11 major actinopterygian clades, and the total number of independent origins of the trait is likely much higher. A principal component analysis revealed that fishes with restricted gill openings occupy a larger morphospace, as defined by our linear measurements, than do fishes with nonrestricted openings. We used a decision tree analysis of ecological data to determine if restricted gill openings are linked to certain environments. We found that fishes with restricted gill openings repeat- edly occur under a variety of ecological conditions, although they are rare in open-ocean pelagic environ- ments. We also tested seven ratios for their utility in dis- tinguishing between fishes with and without restricted gill openings, and we propose a simple metric for quantifying restricted gill openings (RGO), defined as a ratio of the distance from the ventral midline to the gill opening rela- tive to half the circumference of the head. Functional explanations for this specialized morphology likely differ within each clade, but its repeated evolution indicates a need for a better understanding of diversity of ventilatory morphology among fishes. J. Morphol. 000:000-000, 2015.