Phylogenomic analysis of a rapid radiation of misfit fishes (Syngnathiformes) using ultraconserved elements.

Phylogenetics is undergoing a revolution as large-scale molecular datasets reveal unexpected but repeatable rearrangements of clades that were previously thought to be disparate lineages. One of the most unusual clades of fishes that has been found using large-scale molecular datasets is an expanded Syngnathiformes including traditional long-snouted syngnathiform lineages (Aulostomidae, Centriscidae, Fistulariidae, Solenostomidae, Syngnathidae), as well as a diverse set of largely benthic-associated fishes (Callionymoidei, Dactylopteridae, Mullidae, Pegasidae) that were previously dispersed across three orders. The monophyly of this surprising clade of fishes has been upheld by recent studies utilizing both nuclear and mitogenomic data, but the relationships among major lineages within Syngnathiformes remain ambiguous; previous analyses have inconsistent topologies and are plagued by low support at deep divergences between the major lineages. In this study, we use a dataset of ultraconserved elements (UCEs) to conduct the first phylogenomic study of Syngnathiformes. UCEs have been effective markers for resolving deep phylogenetic relationships in fishes and, combined with increased taxon sampling, we expected UCEs to resolve problematic syngnathiform relationships. Overall, UCEs were effective at resolving relationships within Syngnathiformes at a range of evolutionary timescales. We find consistent support for the monophyly of traditional long-snouted syngnathiform lineages (Aulostomidae, Centriscidae, Fistulariidae, Solenostomidae, Syngnathidae), which better agrees with morphological hypotheses than previously published topologies from molecular data. This result was supported by all Bayesian and maximum likelihood analyses, was robust to differences in matrix completeness and potential sources of bias, and was highly supported in coalescent-based analyses in ASTRAL when matrices were filtered to contain the most phylogenetically informative loci. While Bayesian and maximum likelihood analyses found support for a benthic-associated clade (Callionymidae, Dactylopteridae, Mullidae, and Pegasidae) as sister to the long-snouted clade, this result was not replicated in the ASTRAL analyses. The base of our phylogeny is characterized by short internodes separating major syngnathiform lineages and is consistent with the hypothesis of an ancient rapid radiation at the base of Syngnathiformes. Syngnathiformes therefore present an exciting opportunity to study patterns of morphological variation and functional innovation arising from rapid but ancient radiation.

Evolutionary Patterns of Modularity in the Linkage Systems of the Skull in Wrasses and Parrotfish.

The concept of modularity is fundamental to understanding the evolvability of morphological structures and is considered a central framework for the exploration of functionally and developmentally related subsets of anatomical traits. In this study, we explored evolutionary patterns of modularity and integration in the 4-bar linkage biomechanical system of the skull in the fish family Labridae (wrasses and parrotfish). We measured evolutionary modularity and rates of shape diversification of the skull partitions of three biomechanical 4-bar linkage systems using 205 species of wrasses (family: Labridae) and a three-dimensional geometric morphometrics data set of 200 coordinates. We found support for a two-module hypothesis on the family level that identifies the bones associated with the three linkages as being a module independent from a module formed by the remainder of the skull (neurocranium, nasals, premaxilla, and pharyngeal jaws). We tested the patterns of skull modularity for four tribes in wrasses: hypsigenyines, julidines, cheilines, and scarines. The hypsigenyine and julidine groups showed the same two-module hypothesis for Labridae, whereas cheilines supported a four-module hypothesis with the three linkages as independent modules relative to the remainder of the skull. Scarines showed increased modularization of skull elements, where each bone is its own module. Diversification rates of modules show that linkage modules have evolved at a faster net rate of shape change than the remainder of the skull, with cheilines and scarines exhibiting the highest rate of evolutionary shape change. We developed a metric of linkage planarity and found the oral jaw linkage system to exhibit high planarity, while the rest position of the hyoid linkage system exhibited increased three dimensionality. This study shows a strong link between phenotypic evolution and biomechanical systems, with modularity influencing rates of shape change in the evolution of the wrasse skull.

Evolutionary history of the parrotfishes: biogeography, ecomorphology, and comparative diversity.

The family Scaridae comprises about 90 species of herbivorous coral reef, rock reef, and seagrass fishes. Parrotfishes are important agents of marine bioerosion who rework the substrate with their beaklike oral jaws. Many scarid populations are characterized by complex social systems including highly differentiated sexual stages, territoriality, and the defense of harems. Here, we test a hypothesis of relationships among parrotfish genera derived from nearly 2 kb of nuclear and mitochondrial DNA sequence. The DNA tree is different than a phylogeny based on comparative morphology and leads to important reinterpretations of scarid evolution. The molecular data suggest a split among seagrass and coral reef associated genera with nearly 80% of all species in the coral reef clade. Our phylogenetic results imply an East Tethyan origin of the family and the recurrent evolution of excavating and scraping feeding modes. It is likely that ecomorphological differences played a significant role in the initial divergence of major scarid lineages, but that variation in color and breeding behavior has triggered subsequent diversification. We present a two-phase model of parrotfish evolution to explain patterns of comparative diversity. Finally, we discuss the application of this model to other adaptively radiating clades.

Mechanical performance of aquatic rowing and flying.

Aquatic flight, performed by rowing or flapping fins, wings or limbs, is a primary locomotor mechanism for many animals. We used a computer simulation to compare the mechanical performance of rowing and flapping appendages across a range of speeds. Flapping appendages proved to be more mechanically efficient than rowing appendages at all swimming speeds, suggesting that animals that frequently engage in locomotor behaviours that require energy conservation should employ a flapping stroke. The lower efficiency of rowing appendages across all speeds begs the question of why rowing occurs at all. One answer lies in the ability of rowing fins to generate more thrust than flapping fins during the power stroke. Large forces are necessary for manoeuvring behaviours such as accelerations, turning and braking, which suggests that rowing should be found in slow-swimming animals that frequently manoeuvre. The predictions of the model are supported by observed patterns of behavioural variation among rowing and flapping vertebrates.

Ontogeny of feeding motor patterns in infant rats: an electromyographic analysis of suckling and chewing.

During mammalian ontogeny, there is a transition from suckling to the chewing of food. The question was asked: Is suckling a neuromuscular precursor to chewing, or are suckling and chewing independent systems? Electromyograms (EMGs) were recorded in rat pups of ages 6, 9, 12, 15, 18, and 21 days from the superficial masseter, anterior digastric, sternohyoideus, and genioglossus muscles during suckling and chewing. The EMG patterns of the 3 components of suckling behavior (nipple attachment, rhythmic sucking and the stretch response) are distinctive from one another and reflect the musculoskeletal biomechanics of suckling. Chewing EMGs are present by 12 days of age and attain the adult pattern by 18-21 days of age. During nipple attachment, pups exhibit a motor pattern that is similar to that of adult chewing, but other aspects of suckling differ from chewing in some EMG features. Comparison of EMGs between behaviors and between ages allowed interpretation of the degree of contunity of muscular activity across the suckling-to-chewing transition.

Electromyographic analysis of oral habituation in rat pups.

Rat pups show decreases in mouthing activity in response to a series of repeated oral infusions of a diet. This decrease in mouthing activity has been termed "oral habituation" and these changes have been readily recorded with simple behavioral observations. Oral habituation appears to be a component of satiety in young rats. In the present study, to more specifically characterize changes in motor response topography during habituation in muscle groups used for mastication, mouthing activity was recorded by implanting fine wire electromyographic electrodes in the superficial masseter, anterior digastric, sternohyoideus, and genioglossus muscles of 12-day-old rat pups. During testing, pups received a series of brief oral infusions of a 10% sucrose diet delivered through an oral cannula. The results demonstrated that mouthing activity as observed and scored behaviorally was highly correlated with mouthing behavior recorded by EMG, with oral habituation distinctly emerging in both measures. In addition, the pattern of motor activity in the four masticatory muscles changed during the course of oral habituation. Within the minute following a single infusion, the cycle frequency, duration of activity, and relative onset time of activity in the four muscles changed. In addition, across the course of habituation, both cycle frequency and relative onset times of muscle activity changed. These results demonstrate the general reliability of behavioral observations of masticatory motor activity in young rats and provide further information on how the pattern of activity of muscles involved in the mouthing motor pattern is altered during the course of oral habituation.

Motor patterns of herbivorous feeding: electromyographic analysis of biting in the parrotfishes Cetoscarus bicolor and Scarus iseri.

The motor patterns of the herbivorous feeding bite were investigated in two species of parrotfish (Cetoscarus bicolor and Scarus iseri) with functionally distinct biting modes using electromyographic recordings. Behavioral data revealed that S. iseri utilized faster bites, took more bites per feeding bout, and bit at a higher frequency than did C. bicolor. EMGs recorded from the epaxialis (EP), levator operculi (LOP), 3 subdivisions of the adductor mandibulae (A1-A3), and the sternohyoideus (SH) muscles displayed a high degree of within-individual variance. Duration of muscle activity and onset time relative to LOP were shorter in S. iseri than in C. bicolor and S. iseri displayed a greater EMG amplitude in the LOP and SH muscles than did C. bicolor. We calculated the duty factors of the muscles as the relative timing of EMG variables divided by the total feeding cycle time. Patterns of duty factors of the feeding muscles were similar in both species, though muscles were active for a longer portion of the total bite cycle in S. iseri. In addition to its typical bite, S. iseri employed additional motor patterns when taking particularly hard bites. A multivariate comparison of EMGs from biting and suction feeding taxa revealed that the biting motor pattern was significantly different from suction feeding, although there was a high degree of overlap among all feeding strikes. The activity of the sternohyoideus muscle was significantly different between suction feeders and biters. Despite strong similarities of the general motor pattern in a wide range of teleost fishes, components of this pattern are shown to be evolutionarily plastic.

Comparative kinematics of the forelimb during swimming in red-eared slider (Trachemys scripta) and spiny softshell (Apalone spinifera) turtles.

Softshell turtles (Family Trionychidae) possess extensive webbing between the digits of the manus, suggesting that the forelimb may serve as an effective thrust generator during aquatic locomotion. However, the hindlimb has previously been viewed as the dominant propulsive organ in swimming freshwater turtles. To evaluate the potential role of the forelimb in thrust production during swimming in freshwater turtles, we compared the forelimb morphology and three-dimensional forelimb kinematics of a highly aquatic trionychid turtle, the spiny softshell Apalone spinifera, and a morphologically generalized emydid turtle, the red-eared slider Trachemys scripta. Spiny softshells possess nearly twice as much forelimb surface area as sliders for generating drag-based thrust. In addition, although both species use drag-based propulsion, several aspects of forelimb kinematics differ significantly between these species. During the thrust phase of the forelimb cycle, spiny softshells hold the elbow and wrist joints significantly straighter than sliders, thereby further increasing the surface area of the limb that can move water posteriorly and increasing the velocity of the distal portion of the forelimb. These aspects of swimming kinematics in softshells should increase forelimb thrust production and suggest that the forelimbs make more substantial contributions to forward thrust in softshell turtles than in sliders. Spiny softshells also restrict forelimb movements to a much narrower dorsoventral and anteroposterior range than sliders throughout the stroke, thereby helping to minimize limb movements potentially extraneous to forward thrust production. These comparisons demonstrate considerable diversity in the forelimb kinematics of turtles that swim using rowing motions of the limbs and suggest that the evolution of turtle forelimb mechanics produced a variety of contrasting solutions for aquatic specialization.

Kinematics of birdsong: functional correlation of cranial movements and acoustic features in sparrows.

The movements of the head and beak of songbirds may play a functional role in vocal production by influencing the acoustic properties of songs. We investigated this possibility by synchronously measuring the acoustic frequency and amplitude and the kinematics (beak gape and head angle) of singing behavior in the white-throated sparrow (Zonotrichia albicollis) and the swamp sparrow (Melospiza georgiana). These birds are closely related emberizine sparrows, but their songs differ radically in frequency and amplitude structure. We found that the acoustic frequencies of notes in a song have a consistent, positive correlation with beak gape in both species. Beak gape increased significantly with increasing frequency during the first two notes in Z. albicollis song, with a mean frequency for note 1 of 3 kHz corresponding to a gape of 0.4 cm (a 15 degrees gape angle) and a mean frequency for note 2 of 4 kHz corresponding to a gape of 0.7 cm (a 30 degrees gape angle). The relationship between gape and frequency for the upswept third note in Z. albicollis also was significant. In M. georgiana, low frequencies of 3 kHz corresponding to beak gapes of 0.2-0.3 cm (a 10-15 degrees break angle), whereas frequencies of 7-8 kHz were associated with flaring of the beak to over 1 cm (a beak angle greater than 50 degrees). Beak gape and song amplitude are poorly correlated in both species. We conclude that cranial kinematics, particularly beak movements, influence the resonance properties of the vocal tract by varying its physical dimensions and thus play an active role in the production of birdsong.

Modulation of prey capture kinematics in the cheeklined wrasse Oxycheilinus digrammus (Teleostei: Labridae).

The ability to modulate prey capture behaviors is of interest to organismal biologists as it suggests that predators can perceive features of the prey and select suitable behaviors from an available repertoire to successfully capture the item. Thus, behavior may be as important a trait as morphology in determining an organism's diet. Using high-speed video, we measured prey capture kinematics in three cheeklined wrasse, Oxycheilinus digrammus. We studied the effects of three experimental prey treatments: live fish, dead prawn suspended in the water column, and dead prawn pieces anchored to the substrate in a clip. Live prey elicited significantly more rapid strikes than dead prey suspended in the water column, and the head of the predator was expanded to significantly larger maxima. These changes in prey capture kinematics suggest the generation of more inertial suction. With greater expansion of the head, more water can be accelerated into the buccal cavity. The attached prey treatment elicited strikes as rapid as those on live prey. We suggest that the kinematics of rapid strikes on attached prey are indicative of attempts to use suction to detach the prey item. More rapid expansion of the buccal or mouth cavity should lead to higher velocities of water entering the mouth and therefore to enhanced suction. Further modulation in response to the attached prey item, such as clipping or wrenching behaviors, was not observed. J. Exp. Zool. 290:88-100, 2001.