The evolutionary history of reproductive strategies in sculpins of the subfamily oligocottinae

Abstract

The sculpin subfamily Oligocottinae is a group of 17 nearshore species and is noteworthy for the fact that it contains both intertidal and subtidal species, copulating and noncopulating species, and many species with very broad geographic ranges. These factors, as well as the consistency with which the constituent genera have been grouped together historically, make the Oligocottinae an ideal group for the study of the evolution of a reproductive mode known as internal gamete association (IGA), which is unique to sculpins. I conducted a phylogenetic study of the oligocottine sculpins based on an extensive molecular dataset consisting of DNA sequences from eight genomic regions. From the variability present in those sequences, I inferred phylogenetic relationships using parsimony, maximum likelihood, and Bayesian inference. Results of these phylogenetic analyses show that some historical taxonomy and classifications require revision to align taxonomy with evolutionary relatedness. Specifically, the monotypic genus Leiocottus should be synonymized with Clinocottus; membership in the tribe Oligocottini should be reduced to include only the genera Oligocottus, Clinocottus, and Orthonopias; and the genus Sigmistes should be removed from the subfamily Oligocottinae. Using this new phylogenetic framework, I conducted an analysis of the evolution of reproductive behaviors and associated morphological characters in members of Oligocottinae. These traits were obtained through a critical review of the relevant literature and mapped on the phylogeny. Ancestral state reconstruction was used to explore their evolution. The results show that copulation and the presence of an enlarged male genital papilla are likely the ancestral states of Oligocottinae and that these characters were secondarily lost in the lineage composed of Artedius corallinus, A. fenestralis, A. lateralis, and A. notospilotus. The results also show that parental care in the group is split between the Artedius lineage, where males guard egg clutches, and the rest of the group, where egg guarding behavior is not present. I speculate that the differing ecology of these two groups has affected the evolution of reproduction and parental care in the subfamily, where subtidal lineages (i.e., Artedius) engage in parental care but have transitioned away from copulation, while the intertidal lineages maintained copulation but hide their eggs rather than guard them.