Eric J. Hilton

Evolutionary Characters, Phenotypes and Ontologies: Curating Data from the Systematic Biology Literature

Background The wealth of phenotypic descriptions documented in the published articles, monographs, and dissertations of phylogenetic systematics is traditionally reported in a free-text format, and it is therefore largely inaccessible for linkage to biological databases for genetics, development, and phenotypes, and difficult to manage for large-scale integrative work. The Phenoscape project aims to represent these complex and detailed descriptions with rich and formal semantics that are amenable to computation and integration with phenotype data from other fields of biology. This entails reconceptualizing the traditional free-text characters into the computable Entity-Quality (EQ) formalism using ontologies. Methodology/Principal Findings We used ontologies and the EQ formalism to curate a collection of 47 phylogenetic studies on ostariophysan fishes (including catfishes, characins, minnows, knifefishes) and their relatives with the goal of integrating these complex phenotype descriptions with information from an existing model organism database (zebrafish, http://zfin.org). We developed a curation workflow for the collection of character, taxonomic and specimen data from these publications. A total of 4,617 phenotypic characters (10,512 states) for 3,449 taxa, primarily species, were curated into EQ formalism (for a total of 12,861 EQ statements) using anatomical and taxonomic terms from teleost-specific ontologies (Teleost Anatomy Ontology and Teleost Taxonomy Ontology) in combination with terms from a quality ontology (Phenotype and Trait Ontology). Standards and guidelines for consistently and accurately representing phenotypes were developed in response to the challenges that were evident from two annotation experiments and from feedback from curators. Conclusions/Significance The challenges we encountered and many of the curation standards and methods for improving consistency that we developed are generally applicable to any effort to represent phenotypes using ontologies. This is because an ontological representation of the detailed variations in phenotype, whether between mutant or wildtype, among individual humans, or across the diversity of species, requires a process by which a precise combination of terms from domain ontologies are selected and organized according to logical relations. The efficiencies that we have developed in this process will be useful for any attempt to annotate complex phenotypic descriptions using ontologies. We also discuss some ramifications of EQ representation for the domain of systematics.

Skeletal Anatomy of the Shortnose Sturgeon, Acipenser brevirostrum Lesueur, 1818, and the Systematics of Sturgeons (Acipenseriformes, Acipenseridae)

Abstract Sturgeons of the family Acipenseridae comprise 25 extant species, making it the most species-rich extant family of basal (i.e., nonteleostean) actinopterygians. Because of their basal position within Actinopterygii, the anatomical study of sturgeons has a long and rich history, although there remains much to be discovered. Here we describe and illustrate the skeletal anatomy of the shortnose sturgeon, Acipenser brevirostrum, as a representative of the family Acipenseridae. Acipenser brevirostrum, which is distributed along the east coast of North America, is a relatively small species of sturgeon, reaching a maximum of just over 1 m in total length. Our study is based on 105 skeletal and 147 alcohol-stored specimens representing a broad range of ontogenetic stages (ca. 18 to 1000+ mm TL). This study emphasizes the bony portions of the skeleton, their ontogeny, and parts of the skeleton that persist as cartilaginous elements into the adult stage; the earliest stages of development of the chondrocranium, however, will be the subject of a future project. In the present study, we intend to provide baseline data for future comprehensive ontogenetic and morphological studies of Acipenseridae. Although the Acipenseriformes are extremely morphologically derived compared to most basal actinopterygians, these data will be useful in broader systematics studies of basal Actinopterygii generally. Based on previous studies of acipenseriform phylogeny and using new anatomical data collected in this study, we studied the phylogenetic relationships of fossil and living acipenserids. The monophyly of Acipenseriformes is supported by two synapomorphies: palatoquadrates with symphysis between pars autopalatina and the absence of premaxillae and maxillae. Contrary to other recent studies, we recover †Chondrosteus as most basal among Acipenseriformes rather than †Peipiaosteus. †Peipiaosteus + Acipenseroidei is supported by the presence of fewer than seven but more than one branchiostegals, the posterior margin of the branchiostegals serrated, the absence of ossified basibranchials, and the absence of teeth on the gill rakers. Acipenseroidei ( =  Polyodontidae + Acipenseridae) is supported by one synapomorphy (presence of ventral rostral bones). Monophyly of both Polyodontidae and Acipenseridae is well supported. The family Polyodontidae (represented in our analysis by †Protopsephurus and Polyodon) is supported by the presence of well-developed anterior and posterior divisions of the fenestra longitudinalis, the parietals extending posterior to posttemporals, the presence of stellate bones, the ascending process of parasphenoid extending perpendicularly from the lateral margin of the parasphenoid, a serrated posterior margin on the subopercle, and the presence of “microctenoid” scales. The family Acipenseridae is supported by 11 synapomorphies: arching of the rostral canal, a single posteriormost ventral rostral bone, branchiostegals of different shapes, dorsalmost branchiostegal pillar-like and laterally concave, the presence of the palatal complex, an anterior shelf of hypobranchial one, a continuous series of median dorsal scutes extending from skull to dorsal fin, the supracleithrum reaching the level of extrascapulars, a cardiac shield formed by shoulder girdle, the clavicle–cleithrum suture tight and interdigitating, and the presence of a supracleithral cartilage. Within Acipenseridae, we recovered three groupings; Acipenser is not monophyletic. Within Acipenseridae, two supraspecific taxonomic groups are recognized and defined: Husinae (new usage) includes A. ruthenus and Huso huso, and Pseudoscaphirynchinae new subfamily includes A. stellatus and Pseudoscaphirhynchus. Husinae is defined by the frontal bones meeting in midline and a slight medial dermopalatine expansion, although neither of these characters is unique to this clade. Acipenser baerii is more closely related to Husinae than other acipenserids based on the presence of a variable number of distinctly raised prominences on the ventral rostral bones but is excluded from the subfamily pending further study, including denser taxon sampling within Acipenser. The new subfamily Pseudoscaphirynchinae is defined by having the horizontal arm of jugal bone undercut the nasal capsule, a uniquely derived character. Although suitable specimens of all species of Acipenseridae were not available, we note that this is the first robust morphological phylogenetic study addressing species-level relationships for this family, and we hope our study will serve as a baseline study for future comparative anatomical and systematic studies of Acipenseridae.

Redescription of †Chondrosteus acipenseroides Egerton, 1858 (Acipenseriformes, †Chondrosteidae) from the lower Lias of Lyme Regis (Dorset, England), with comments on the early evolution of sturgeons and paddlefishes

Synopsis We present a redescription of †Chondrosteus acipenseroides, a basal member of the order Acipenseriformes (sturgeons, paddlefishes and their fossil relatives) from the Lower Jurassic of England. †Chondrosteus is known from several whole or partial skeletons and many isolated fragmentary elements. Even on many of the articulated skeleton and skull specimens, many aspects of its anatomy are not sufficiently preserved to allow for detailed descriptions. However, we were able to describe it more fully than previous authors and to clarify many points of anatomy, such as the presence of elements we interpret as rostral canal bones, the absence of a postorbital bone, the sclerotic ring being composed of dorsal and ventral elements, a deep lateral groove on the dentary and the presence of an ossified basibranchial. We then comment on the systematic affinities of †Chondrosteidae within Acipenseriformes on the basis of the results of a new phylogenetic analysis. †Chondrosteidae has alternatively been regarded as the sister‐group of all other Acipenseriformes (i.e. †Peipiaosteidae + Acipenseridae + Polyodontidae) or the sister‐group of Acipenseridae + Polyo‐dontidae. Our new systematic analysis supports the former hypothesis. All Acipenseriformes to the exclusion of †Chondrosteidae is supported by the following synapomorphies: fewer than seven but more than one branchiostegal, the absence of ossified basibranchials, and the absence of teeth on the gill rakers.

Seasonal Distributions and Movements of Longnose Gar (Lepisosteus osseus) within the York River System, Virginia

Abstract The seasonal movements of Lepisosteus osseus (Longnose Gar) are largely unknown. The goal of this project was to characterize spawning movements and seasonal distributions by using acoustic tagging methods and examining historical catch records from a trawl survey. This is the first time that movements have been studied for an estuarine population of Longnose Gar. Two individuals moved greater minimum distances (69 and 74 km) than found in the only other report on movement in this species. Spawningground residency time, collected from two tagged Longnose Gar, was approximately one month, and tidal periodicity was observed for one of the two fish. Data from a fisheries independent trawl survey were used to examine seasonal catch distributions in Longnose Gar and represents the first report of winter distributions for this species. Winter locations occurred both alongshore and mid-channel, and the distributions were similar to those in the summer and fall.

A Replacement Name for †Psammorhynchus Grande & Hilton, 2006 (Actinopterygii, Acipenseriformes, Acipenseridae)

In 2006, we (Grande & Hilton, 2006) described a well-preserved fossil sturgeon (Acipenseridae) from the Late Cretaceous of Montana and proposed the name † Psammorhynchus longipinnis Grande & Hilton for the new species. Through accidental discovery of an on-line taxonomic database of flatworms (Tyler et al., 2006) and subsequent investigation, we recently discovered that the genus-group name is preoccupied by Psammorhynchus Meixner, 1938 in Platyhelminthes (“Turbellaria”). Therefore, under Article 60 of the International Code of Zoological Nomenclature (ICZN, 1999), a replacement name is required for the junior homonym † Psammorhynchus Grande and Hilton. ### Genus † Priscosturion nom. nov #### Type species † Psammorhynchus longipinnis Grande & Hilton, 2006 (= …

Osteology of the Graveldiver Scytalina cerdale (Perciformes: Zoarcoidei: Scytalinidae).

The Graveldiver, Scytalina cerdale, is a small, poorly known burrowing fish from the intertidal and subtidal zones of the west coast of North America, ranging from south‐central California to Alaska. This is the sole member of the family Scytalinidae, which is included in the Zoarcoidei. Although it was described over 120 years ago, it is rare in natural history collections and its anatomy is only imperfectly known. This article describes and illustrates the skeletal anatomy of S. cerdale based on newly prepared cleared and stained specimens. Many points of its anatomy are clarified or corrected (e.g., presence of the intercalars and ribs, in contrast to their reported absence) or described for the first time (e.g., structure of its gill‐arches). Previous hypotheses of its systematic placement within the Zoarcoidei are discussed. On the basis of preliminary comparisons, S. cerdale may have phylogenetic affinity with at least some members of the family Stichaeidae (e.g., Xiphister). However, further study is needed on the anatomy and inter‐relationships of the families of the Zoarcoidei before any conclusions can be made. J. Morphol., 2009.

Anatomy and early development of the pectoral girdle, fin, and fin spine of sturgeons (Actinopterygii: Acipenseridae)

Acipenseriformes hold an important place in the evolutionary history of bony fishes. Given their phylogenetic position as extant basal Actinopterygii, it is generally held that a thorough understanding of their morphology will greatly contribute to the knowledge of the evolutionary history and the origin of diversity for the major osteichthyan clades. To this end, we examined comparative developmental series from the pectoral girdle in Acipenser fulvescens, A. medirostris, A. transmontanus, and Scaphirhynchus albus to document, describe, and compare ontogenetic and allometric differences in the pectoral girdle. We find, not surprisingly, broad congruence between taxa in the basic pattern of development of the dermal and chondral elements of the pectoral girdle. However, we also find clear differences in the details of structure and development among the species examined in the dermal elements, including the clavicle, cleithrum, supracleithrum, posttemporal, and pectoral‐fin spine. We also find differences in the internal fin elements such as the distal radials as well as in the number of fin rays and their association with the propterygium. Further, there are clear ontogenetic differences during development of the dermal and chondral elements in these species and allometric variation in the pectoral‐fin spine. The characters highlighted provide a suite of elements for further examination in studies of the phylogeny of sturgeons. Determining the distribution of these characters in other sturgeons may aid in further resolution of phylogenetic relationships, and these data highlight the role that ontogenetic and comparative developmental studies provide in systematics. J. Morphol. 276:241–260, 2015.

Comparative ontogeny of the feeding apparatus of sympatric drums (Perciformes: Sciaenidae) in the Chesapeake Bay.

The anatomy of the feeding apparatus in fishes, including both oral and pharyngeal jaw elements, is closely related to the ecology of a species. During ontogeny, the oral and pharyngeal jaws undergo dramatic changes. To better understand how such ontogenetic changes occur and relate to the feeding ecology of a species, ontogenetic series of four closely related members of the family Sciaenidae (Cynoscion nebulosus, Cynoscion regalis, Micropogonias undulatus, and Leiostomus xanthurus) were examined. Sciaenids were selected because as adults they exhibit considerable specialization of the feeding apparatus correlated with differences in foraging habitats. However, it is not clear when during ontogeny the structural specializations of the feeding apparatus develop, and thereby enable early life history stage (ELHS) sciaenids to partition their foraging habitats. A regression tree was recovered from the analysis and three divergences were identified during ontogeny. There are no measurable differences in elements of the feeding apparatus until the first divergence at 8.4 mm head length (HL), which was attributed to differences in average gill filament length on the second ceratobranchial. The second divergence occurred at 14.1 mm HL and was associated with premaxilla length. The final divergence occurred at 19.8 mm HL and was associated with differences in the toothed area of the fifth certatobranchial. These morphological divergences suggest that ELHS sciaenids may be structurally able to partition their foraging habitats as early as 8.4 mm HL. J. Morphol. 277:183–195, 2016.

Development of the skull and pectoral girdle in Siberian sturgeon, Acipenser baerii, and Russian sturgeon, Acipenser gueldenstaedtii (Acipenseriformes: Acipenseridae)

The head is considered the major novelty of the vertebrates and directly linked to their evolutionary success. Its form and development as well as its function, for example in feeding, is of major interest for evolutionary biologists. In this study, we describe the skeletal development of the cranium and pectoral girdle in Siberian (Acipenser baerii) and Russian sturgeon (A. gueldenstaedtii), two species that are commonly farmed in aquaculture and increasingly important in developmental studies. This study comprises the development of the neuro‐, viscero‐ and dermatocranium and the dermal and chondral components of the pectoral girdle, from first condensation of chondrocytes in prehatchlings to the early juvenile stage and reveals a clear pattern in formation. The otic capsules, the parachordal cartilages, and the trabeculae cranii are the first centers of chondrification, at 8.4mm TL. These are followed by the mandibular, then the hyoid, and later the branchial arches. Teeth form early on the dentary, dermopalatine, and palatopterygoid, and then appear later in the buccal cavity as dorsal and ventral toothplates. With ongoing chondrification in the neurocranium a capsule around the brain and a strong rostrum are formed. Dermal ossifications start to form before closure of the dorsal neurocranial fenestrae. Perichondral ossification of cartilage bones occurs much later in ontogeny. Our results contribute data bearing on the homology of elements such as the lateral rostral canal bone that we regard homologous to the antorbital of other actinopterygians based on its sequence of formation, position and form. We further raise doubts on the homology of the posterior ceratobranchial among Actinopteri based on the formation of the hyoid arch elements. We also investigate the basibranchials and the closely associated unidentified gill‐arch elements and show that they are not homologous. J. Morphol. 278:418–442, 2017.

Shifts of sensory modalities in early life history stage estuarine fishes (Sciaenidae) from the Chesapeake Bay using X-ray micro computed tomography

Increases in human populations along coasts have altered the estuarine nursery habitats that are important for many aquatic organisms. These perturbations include changes to the sensory environment due to increased turbidity resulting from runoff and nutrient loading; these changes are occurring faster than fish species can become adapted to the new prevailing conditions. However, understanding how modifications to the sensory environment impacts fishes during early life history stages (ELHS) requires understanding the senses used to locate food and evade predators and how they change during ontogeny. The drums (Sciaenidae) exhibit substantial morphological diversity in their peripheral sense organs as adults. We, therefore, used the relative volumes of their brain structures to assess ontogenetic changes in the sensory modalities of sciaenid species from different foraging guilds. Early stage sciaenids were imaged using X-ray micro computed tomography. The optic tract was the largest sensory region, suggesting that vision is the primary sensory modality in sciaenids, regardless of size, species, or foraging habitat. There were differences in the relative proportions of the other sensory areas according to foraging guild. These differences suggest that Cynoscion nebulosus (a pelagic forager) relies on audition and mechanoreception through ontogeny to augment vision, whereas Sciaenops ocellatus (a generalist forager) uses olfaction, audition, and mechanoreception. In contrast, Leiostomus xanthurus (a benthic forager) relies on olfaction and gustation. We propose that the ontogenetic trends in sensory modality described in sciaenids from the Chesapeake Bay (USA) can be used in future research to ascertain the potential species-specific impacts of water quality change on ELHS fishes.