Evolution of Feeding-Associated Morphology in Etheostomatinae (Darter Fishes)

Abstract

Biologists have long tried to understand the inequal distribution of diversity across the tree of life. Some species have conserved morphology over time, while others have diversified, some to the very extremes of morphology. Etheostomatinae, a radiation of freshwater fishes, is a speciose clade (approximately 240 species) that shows impressive diversity in skull and jaw morphology. I quantified the morphological disparity and functional diversity of feeding-associated traits across the darter radiation using updated and non-destructive methods. Using µCT and diceCT scanning, I created a set of three-dimensional models of the skull and associated musculature of 88 species of darters (N = 233). Skull components were analyzed using 3D geometric morphometrics and this data set, along with muscle volume measurements, was used to calculate five biomechanical indices known to influence feeding strategy in fishes: opening jaw MA (mechanical advantage), closing jaw MA, oral jaw KT (kinematic transmission), hyoid KT, and adductor mandibulae volume. I found morphological diversity in darters was most strongly impacted by mouth size and position and head elongation, while jaw closing lever mechanics, jaw muscle size, and hyoid kinematics were important for differentiating the major clades of darters. I found evidence for an early burst model of evolution based on skull elongation, along with multiple overlapping early evolutionary shifts in form and function, including for previously identified ecomorphs (e.g., rock flippers and manipulators). I also found the relationship between form and function to be strong and significant across all darters and when considering some of the major clades individually (Etheostoma and Percina), though species in highly specialized, energetic habitats appear to have weaker form-function relationships. The evolution of the cranium of darters appears to have been initially impacted by adaptive divergence between midwater darters and those inhabiting soft-substrate environments and strongly benthic species living in fast water, rocky habitats. Subsequent adaptive shifts appear to be focused on adaptation to foraging in different microhabitats (e.g., over top of, vs. under rocks). Foraging trade-offs appear to be strongly correlated with form-function relationships and may have been impacted by constructional constraints on body elongation in darters, especially in fast water habitats. My work suggests that ecological adaptation has played an important role in generating the morphological diversity of the darter clade.