Beaks promote rapid morphological diversification along distinct evolutionary trajectories in labrid fishes (Eupercaria: Labridae).

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.

Burrowing constrains patterns of skull shape evolution in wrasses.

The evolution of behavioral and ecological specialization can have marked effects on the tempo and mode of phenotypic evolution. Head-first burrowing has been shown to exert powerful selective pressures on the head and body shapes of many vertebrate and invertebrate taxa. In wrasses, burrowing behaviors have evolved multiple times independently, and are commonly used in foraging and predator avoidance behaviors. While recent studies have examined the kinematics and body shape morphology associated with this behavior, no study to-date has examined the macroevolutionary implications of burrowing on patterns of phenotypic diversification in this clade. Here, we use three-dimensional geometric morphometrics and phylogenetic comparative methods to study the evolution of skull shape in fossorial wrasses and their relatives. We test for skull shape differences between burrowing and non burrowing wrasses and evaluate hypotheses of shape convergence among the burrowing wrasses. We also quantify rates of skull shape evolution between burrowing and non burrowing wrasses to test for whether burrowing constrains or accelerates rates of skull shape evolution in this clade. We find that while burrowing and non burrowing wrasses exhibit similar degrees of morphological disparity, for burrowing wrasses, it took nearly twice as long to amass this disparity. Furthermore, while the disparities between groups are evenly matched, we find that most burrowing species are confined to a particular region of shape space with most species exhibiting narrower heads than many non-burrowing species. These results suggest head-first burrowing constrains patterns of skull shape diversification in wrasses by potentially restricting the range of phenotypes that can perform this behavior.

Mosaic Evolution of the Skull in Labrid Fishes Involves Differences in Both Tempo and Mode of Morphological Change.

Modularity is a ubiquitous feature of organismal design that plays an important role in structuring patterns of morphological diversification. Modularity can facilitate evolutionary changes by allowing subsets of traits to coevolve as integrated units and follow quasi-independent evolutionary trajectories, a pattern that may be particularly consequential in the case of highly complex morphological structures. Here we examine modularity in a complex and highly kinetic structure, the teleost skull, and ask if a modular organization of the skull has influenced the diversification dynamics of the shapes of its osteological components across the labrid phylogeny. We compiled one of the largest 3D morphological data sets of fishes to date and used geometric morphometrics to quantify patterns of cranial shape evolution across 184 species of wrasses (Labridae). We then tested several hypotheses of modularity inspired by functional and developmental relationships between cranial bones and compared phenotypic rates among modules. We also compared the fit of models of trait evolution for the entire skull and the various articulated bones that it comprises. Our analyses indicated strong support for a 2-module hypothesis, one that encompasses the oral and pharyngeal jaws and another module comprised of the neurocranium, hyoid apparatus, and operculum. This functional hypothesis yielded one of the highest significant rate differentials across modules, yet we also found that the best-fitting models of trait evolution differed among skull bones. These results suggest that modularity can influence morphological diversification in complex biological structures via differences in both the tempo and mode of evolutionary change. [3D geometric morphometrics, cranial morphology, evolutionary modularity, Labridae, phenotypic rates, structural complexity.].

Suction feeding of West African lungfish (Protopterus annectens): An XROMM analysis of jaw mechanics, cranial kinesis, and hyoid mobility.

Suction feeding in fishes is characterized by rapid cranial movements, but extant lungfishes (Sarcopterygii: Dipnoi) exhibit a reduced number and mobility of cranial bones relative to actinopterygian fishes. Despite fusion of cranial elements, lungfishes are proficient at suction feeding, though the impacts of novel cranial morphology and reduced cranial kinesis on feeding remain poorly understood. We used X-ray reconstruction of moving morphology (XROMM) to study the kinematics of seven mobile elements (neurocranium, upper jaw, lower jaw, tongue, ceratohyal, clavicle, and cranial rib) and two muscles (costoclavicular portion of the hypaxialis and rectus cervicis) during the feeding strikes of West African lungfish (Protopterus annectens). We found that feeding by P. annectens on non-evasive prey is relatively slow, with a mean time to peak gape of 273 ms. Lower jaw depression and clavicular rotation were hinge-like, with one degree of freedom, but the ceratohyals rotated in a complex motion involving depression and long-axis rotation. We quantified the relative contributions to oral cavity volume change (RCVC) and found that oral cavity expansion is created primarily by ceratohyal and clavicle motion. P. annectens suction feeds relatively slowly but successfully through muscle shortening of hypaxial and rectus cervicis muscles contributing to hyoid mobility.

Air Breathing and Suction Feeding Kinematics in the West African Lungfish, Protopterus annectens.

Research on the water-to-land transition tends to focus on the locomotor changes necessary for terrestriality. However, the evolution from water breathing to air breathing was also a necessary precursor to the invasion of land. Air is approximately 1000 times less dense and 50 times less viscous, and contains hundreds of times more oxygen than water. However, unlike the transition to terrestrial locomotion, breathing air does not require body weight support, so the evolution of air breathing may have necessitated smaller changes to morphology and function. We used X-ray reconstruction of moving morphology to compare the cranial kinematics of aquatic buccal pumping, such as that seen in suction feeding, with the aerial buccal pumping required for lung ventilation in the West African lungfish (Protopterus annectens). During buccal pumping behaviors, the cranial bones and associated soft tissues act as valves and pumps, and the sequence of their motions controls the pattern of fluid flow. Both behaviors are characterized by an anterior-to-posterior wave of expansion and an anterior-to-posterior wave of compression. We found that the pectoral girdle and cranial rib rotate consistently during air breathing and suction feeding, and that the muscle between them shortens during buccal expansion. Overall, we conclude that the major cranial bones maintain the same basic functions (i.e., acting as valves or pumps, or transmitting power) across aquatic and aerial buccal pumping. The cranial morphology that enables aquatic buccal pumping is well suited to perform air breathing and accommodates the physical differences between air and water.

Effects of Diet and Intraspecific Scaling on the Viscera of Muraenid Fishes.

Diet has a strong influence on the morphology and physiology of vertebrates. Members of numerous fish clades have provided excellent comparative models for examining the effects of diet, primarily carnivory vs. herbivory, on organ systems. In this study, we comparatively examined the effects of carnivory, specifically independent evolutions of piscivory and durophagy, on body dimensions, organ topology, and organ proportions between nine moray species (Muraenidae). We found that organ placement via the anteroposterior organ positions differed between members in the two diet categories, although general organ topology is conserved. The stomach (31 - 55%) and intestine (68 - 76%) consistently occupied the majority of the body cavity irrespective of diet. Diet was shown to influence overall body dimensions and relative organ proportions across all moray species. Durophagous morays have shorter head lengths and body depths, and shorter heart, liver, gall bladder, and spleen lengths compared to piscivorous species. There was also greater variation in organ lengths among durophagous species than within piscivorous species. We attribute this greater variation in organ lengths to the multiple independent origins of durophagy within Muraenidae. Our single intraspecific comparison of the California moray, Gymnothorax mordax, a piscivorous species, revealed that all organs scale isometrically with body cavity length over ontogeny. The stomach grows proportionally with body cavity length and is the second longest organ in G. mordax at all ontogenetic stages, with the longest being the intestine. This suggests that morays can consume large quantities of prey or relatively large individual prey throughout their life history. In addition to scaling patterns of G. mordax, our study is the first to investigate the effects of diet and the intraspecific scaling patterns on the viscera of members of the Muraenidae, a clade of obligate carnivores that inhabit most marine ecosystems.