The teleost anatomy ontology: anatomical representation for the genomics age

Abstract

The rich knowledge of morphological variation among organisms reported in the systematic literature has remained in free-text format, impractical for use in large-scale synthetic phylogenetic work. This noncomputable format has also precluded linkage to the large knowledgebase of genomic, genetic, developmental, and phenotype data in model organism databases. We have undertaken an effort to prototype a curated, ontology-based evolutionary morphology database that maps to these genetic databases (http://kb.phenoscape.org) to facilitate investigation into the mechanistic basis and evolution of phenotypic diversity. Among the first requirements in establishing this database was the development of a multispecies anatomy ontology with the goal of capturing anatomical data in a systematic and computable manner. An ontology is a formal representation of a set of concepts with defined relationships between those concepts. Multispecies anatomy ontologies in particular are an efficient way to represent the diversity of morphological structures in a clade of organisms, but they present challenges in their development relative to single-species anatomy ontologies. Here, we describe the Teleost Anatomy Ontology (TAO), a multispecies anatomy ontology for teleost fishes derived from the Zebrafish Anatomical Ontology (ZFA) for the purpose of annotating varying morphological features across species. To facilitate interoperability with other anatomy ontologies, TAO uses the Common Anatomy Reference Ontology as a template for its upper level nodes, and TAO and ZFA are synchronized, with zebrafish terms specified as subtypes of teleost terms. We found that the details of ontology architecture have ramifications for querying, and we present general challenges in developing a multispecies anatomy ontology, including refinement of definitions, taxon-specific relationships among terms, and representation of taxonomically variable developmental pathways.

FIGURE 1.

Three-dimensional model of the Weberian apparatus of the zebrafish Danio rerio in lateral view, anterior to left. The specimen is deposited at Academy of Natural Sciences, Philadelphia, ANSP 189304, standard length = 25.5 mm. The specimen was embedded in agarose gel and scanned at low voltage (30 kV) and high amperage (181 A) on the Skyscan 1172 Microfocus X-radiographic Scanner in laboratory of Dr. J. W. Hagadorn at Amherst College, Amherst, MA. The three-dimensional image processing was done with the software VGStudio MAX v.1.2.1 (Volume Graphics, Heidelberg, Germany) at the Department of Ichthyology, ANSP.

FIGURE 2.

Graphical representation of the Weberian apparatus and its parts in the TAO. Term names are enclosed in ovals; definitions shown in Table 1. Relationships between terms are shown as lines: is_a (red), part_of (blue), and develops_from (green). The dashed lines represent taxonomically variable is_a and part_of relationships (i.e., vertebra 1–4 are types of Weberian vertebra only in otophysan fishes, Fig. 1 and text). Not all relationships are illustrated.

FIGURE 3.

The process of updating TAO to include new terms, refined definitions, synonym additions, and structural changes begins with term requests from ontology users through the SourceForge Term Tracker (http://sourceforge.net/tracker/?group_id=76834&atid=994764). Requests trigger an automated e-mail to the ichthyological community through the teleost-discuss mailing list (https://lists.sourceforge.net/lists/listinfo/obo-teleost-discuss). Discussion ensues, a decision is reached, and the request is summarized by the TAO administrator on the tracker page. The request is then closed, and TAO is updated to include the requested change. Updates that also apply to the ZFA are made during synchronization.

FIGURE 4.

Representation of the subtypes of vertebra in a) ZFA and b) TAO. Danio rerio exhibits a modal number of 4 Weberian vertebra, 10 precaudal vertebra, and 17 caudal vertebra (Bird and Mabee 2003), and precaudal vertebra and caudal vertebra may be represented as intermediate nodes in the ZFA (a), whereas they are necessarily leaf nodes in TAO (b) because of variability in number of each type of vertebra among teleost species. Not all individual, numbered vertebra are represented in ZFA and TAO.

FIGURE 5.

Multiple developmental pathways of the sublingual represented in the TAO. The sublingual is a median element of the lower hyoid arch in cypriniform fishes. In at least one species, the ossified sublingual (sublingual dorsal and ventral fused) results from the fusion of 2 cartilage elements, whereas in other species, the sublingual exists as separate ossified elements (sublingual dorsal and ventral separate). These terms have different is_a parents due to structural differences.