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Abstract Evolutionary innovations have played an important role in shaping the diversity of life on Earth. However, how these innovations arise and their downstream effects on patterns of morphological diversification remain poorly understood. Here, we examine the impact of evolutionary innovation on trait diversification in tetraodontiform fishes (pufferfishes, boxfishes, ocean sunfishes, and allies). This order provides an ideal model system for studying morphological diversification owing to their range of habitats and divergent morphologies, including the fusion of the teeth into a beak in several families. Using three-dimensional geometric morphometric data for 176 extant and fossil species, we examine the effect of skull integration and novel habitat association on the evolution of innovation. Strong integration may be a requirement for rapid trait evolution and facilitating the evolution of innovative structures, like the tetraodontiform beak. Our results show that the beak arose in the presence of highly conserved patterns of integration across the skull, suggesting that integration did not limit the range of available phenotypes to tetraodontiforms. Furthermore, we find that beaks have allowed tetraodontiforms to diversify into novel ecological niches, irrespective of habitat. Our results suggest that general rules pertaining to evolutionary innovation may be more nuanced than previously thought. 

Abstract The upper and lower jaws of some wrasses (Eupercaria: Labridae) possess teeth that have been coalesced into a strong durable beak that they use to graze on hard coral skeletons, hard-shelled prey, and algae, allowing many of these species to function as important ecosystem engineers in their respective marine habitats. While the ecological impact of the beak is well understood, questions remain about its evolutionary history and the effects of this innovation on the downstream patterns of morphological evolution. Here we analyze 3D cranial shape data in a phylogenetic comparative framework and use paleoclimate modeling to reconstruct the evolution of the labrid beak across 205 species. We find that wrasses evolved beaks three times independently, once within odacines and twice within parrotfishes in the Pacific and Atlantic Oceans. We find an increase in the rate of shape evolution in the Scarus+Chlorurus+Hipposcarus (SCH) clade of parrotfishes likely driven by the evolution of the intramandibular joint. Paleoclimate modeling shows that the SCH clade of parrotfishes rapidly morphologically diversified during the middle Miocene. We hypothesize that possession of a beak in the SCH clade coupled with favorable environmental conditions allowed these species to rapidly morphologically diversify. 

During ontogeny, animals often undergo significant shape and size changes, coinciding with ecological shifts. This is evident in parrotfishes (Eupercaria: Labridae), which experience notable ecological shifts during development, transitioning from carnivorous diets as larvae and juveniles to herbivorous and omnivorous diets as adults, using robust beaks and skulls for feeding on coral skeletons and other hard substrates. These ontogenetic shifts mirror their evolutionary history, as parrotfishes are known to have evolved from carnivorous wrasse ancestors. Parallel shifts at ontogenetic and phylogenetic levels may have resulted in similar evolutionary and ontogenetic allometric trajectories within parrotfishes. To test this hypothesis, using micro-computed tomography (μCT) scanning and three-dimensional geometric morphometrics, we analyse the effects of size on the skull shape of the striped parrotfishScarus iseriand compare its ontogenetic allometry to the evolutionary allometries of 57 parrotfishes and 162 non-parrotfish wrasses. The youngS. iserihave skull shapes resembling non-parrotfish wrasses and grow towards typical adult parrotfish forms as they mature. There was a significant relationship between size and skull shapes and strong evidence for parallel ontogenetic and evolutionary slopes in parrotfishes. Our findings suggest that morphological changes associated with the ecological shift characterizing interspecific parrotfish evolution are conserved in their intraspecific ontogenies.