Using ontology-based reasoning to integrate taxon and gene phenotypes, the team has demonstrated the discovery of candidate genes underlying evolutionarily novel phenotypes (Edmunds et al. 3). Bastian F., Parmentier G., Roux J., Moretti S., Laudet V., Robinson-Rechavi M.. However, given the size of the anatomy and phenotype ontologies used by Phenoscape, even with REA, OWL reasoning on the complete terminology is only feasible using fast EL reasoners such as ELK (Kazakov et al. . As its name states, REA models a homology annotation as a reciprocal pair of axioms. In addition, the AVA model also returned the specified query term and any subtypes, because the query term is itself a descendant of the ancestral structure in the model. Drosophila, dorsal appendage primordia (wing and haltere imaginal discs) are induced during embryogenesis. What Bridges found was a partial mutation in Ubx. vg-dependent epidermal tissues that contribute to the adult morphology in the non-winged segments. It is used primarily for automated quality control of annotations and for consistency checking when merging independently developed anatomy ontologies into Uberon. . 44, For each competency question, we added a named class expression to this OWL file for the purpose of allowing an automated reasoner to infer subsumption of phenotype instances. Although the AVA model more closely meets our personas expectations for the competency questions, its reliance on more expressive OWL reasoning prohibits its use in practice, e.g., at the scale of a knowledgebase such as the Phenoscape KB. Further, because proposals of homology are tested by concordance with phylogeny, to the extent that phylogenetic hypotheses themselves are in flux, hypotheses of homology are as well. Phenotype ontologies: are homology relations central enough? 2014. The .gov means its official. 5, Bone of the dorsal hyoid arch, references some bone in a region and is not more informative than an ontological parent class expression such as endochondral bone that is part of or derived from the hyoid arch skeleton. That is, in the binary representation, the homologs are also connected to a more general anatomical class, but there it is implied by the structure of the ontology and is thus not necessarily an evolutionary concept. If different species share common ancestors, we would expect organisms to share similarities inherited from those ancestors. 2016) and the use of semantic similarity to discover evolutionary variation related to gene phenotypes (Manda et al. View the full answer. 1Department of Biology, Miami University, Pearson Hall, 700E High Street, Oxford, OH 45056, USA, 2Division of Evolutionary Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka Myodaiji, Okazaki 444-8585, Japan, 3Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), 38 Nishigonaka Myodaiji, Okazaki 444-8585, Japan. This is the case even for serial homologs. As discussed in the previous section, tissue function can diverge among serially homologous structures, which means that the expression of the first class of marker genes likely differs even among serially homologous tissues if the function of these tissues is different. Biology BMC Biology Hox genes modify serial homology patterns in many organisms, exemplified in vertebrates by modification of the axial skeleton and in arthropods by diversification of the body segments. For example, although it is accepted that the paired fins of fishes are homologous to the limbs of terrestrial vertebrates, when this statement is translated into a homology assertion (paired fin homologous_to limb), the queries involving the more specific subtypes of these terms yield some results that are more general than expected. Embryological evidence identifies wing digits in birds as digits 1, 2, and 3, Integration of anatomy ontologies and evo-devo using structured Markov models suggests a new framework for modeling discrete phenotypic traits. The third mode (Hox action 3) is rather unique since Dll expression At least in However, some classic studies hint that it may be worth applying at least some of these approaches to non-model insects. Because each profile omits different capabilities, each is better suited to particular kinds of modeling tasks. Another intriguing approach is to induce a wing serial homologs-to-wing transformation series. 2) and Competency Question 7 (query for serial homologs of hind flipper, Fig. Our motivation for undertaking this work, and the context in which we test different formalisms, is the Phenoscape project (phenoscape.org), in which we have been working to demonstrate the value of a semantic approach through the development of multispecies anatomy ontologies (Dahdul et al. 2015. Because of this lack of homology correspondence across biological levels, the desired outcome from a query for historical homologs of pectoral fin bud would be forelimb bud or forelimb wing bud, but not the product of further bud development, that is, forelimb or forelimb wing. Vice versa, the desired outcome from a query for historical homologs of pectoral fin would be forelimb and its subtype forelimb wing, but not their developmental precursors forelimb bud and forelimb wing bud.. Myoblast diversification and ectodermal signaling in. Our persona expects a query for historical homologs of pectoral fin bud to return phenotypes for forelimb bud and its subtype forelimb wing bud (Fig. Note that this file is intended to be used in conjunction with referenced ontologies (e.g., Uberon) and includes only the homology axioms, not metadata for individual terms such as label and definition. Drosophila situation likely does not reflect an ancestral state. In the Phenoscape KB, for example, the more computationally feasible REA model of homology was implemented. 2013. vg expression will be useful as the first step to identify potential wing serial homologs, but it is also important to analyze the expression of additional wing marker genes. REA did not return any results from a query for homologs of forelimb wing. The same AVA query returned all expected results and additionally phenotypes for the search term itself (forelimb wing; Fig. They do not expect the query to return the superclass of the search term (hindlimb), structures for parts (e.g., humerus, femur) of the serial homologs, historical homologs (e.g., pectoral fin) of the serial homologs, or developmental precursors (e.g., hindlimb bud, forelimb bud) of the serial homologs. Since there are no obvious wing-like structures outside of the second and third thoracic segments (T2 and T3) in insects, only a handful of structures (such as mayfly gills and termite paranotal expansions) have been proposed to be wing serial homologs 51. sharing sensitive information, make sure youre on a federal The application of molecular and functional approaches (an evo-devo approach) may allow us to identify hidden wing serial homologs in wingless segments, which could provide us with critical information to unveil the origin of insect wings. For example distal-less regulates outgrowth of the limbs of insects and vertebrates, but phylogenies nearly conclusively reflect the independent evolution of limbs in these taxa (i.e., that they are not historical homologs; Panganiban et al. In the head segments, these appendages form a series of mouthparts as well as antennae. 2016). Drosophila, some of which may be used as additional wing markers. For example, it has been reported that wing tissue arises at a lateral (pleural) position and migrates dorsally to merge into the tergolateral margin during the nymphal stages in a dragonfly, which may support the pleural (or perhaps dual?) 21, further supporting the idea that the presence of serial homologs corresponds to the expression of marker genes. Morphogens, compartments, and pattern: lessons from drosophila? 5. The complexity of anatomical data, however, has been an impediment to standardization and computation, and many of the critical tasks rely on manual inspection of the data and human judgment (Vogt 2018a). What is serial homology and why is it helpful to understand the origin of insect wings? We assembled a collection of homology assertions from the literature with a set of taxon phenotypes for the skeletal elements of vertebrate fins and limbs from the Phenoscape Knowledgebase. These grouping classes do not affect the outcome of the reasoning (see Supplementary materials S3 available on Dryad; see Software and Data Availability section). National Library of Medicine Results expected by our biologist persona and the results obtained under REA and AVA models for competency questions 17. There is a growing body of research on the evolution of anatomy in a wide variety of organisms. Our goal with this study is to understand the ramifications of different ways of representing historical and serial homology for anatomical entities as a set of ontology axioms. Classes of homology from this ontology are mirrored as object properties within RO, providing the relationships needed to assert historical or serial homology between anatomical structures. 2010. 4. In the REA model, the expected results were not returned for Competency Question 2 (query for historical homologs of forelimb wing, Fig. Although some expectations are clear, and would be so to any biologist (e.g., that the parts of homologous structures are not necessarily homologs), others might be debatable. 2012). Most often these properties involve structural criteria but developmental and functional ones are employed, too. 2016. The longer tradition of comparative anatomy has also revealed extensive conservation, with the homologies between the jaw bones of fishes and the inner ear bones of mammals as a quintessential example. Homology statements were annotated using the appropriate ontologies: anatomy terms using the Uberon anatomy ontology (Haendel et al. The merger of these two wing serial homologs (both tergal and pleural) appears to be essential for the formation of ectopic wings upon Hox LOF mutation, suggesting a dual origin of insect wings Enabling individualized selection of homology relationships would alter the reasoning and thus the derivative products of knowledgebases. Examples would be part_of or develops_from.. The origin and development of the wings of Coleoptera. Hox genes are the region selectors responsible for the individualization of the otherwise uniform segments and segmentally repetitive structures (that is, serial homologs) 2010. Terms for types of phylogenetic evidence (ECO: 0000080) that support homology are available in ECO, though not applicable to the literature referenced in relation to the terms included herein (Supplementary material S1 available on Dryad). . Below, we will discuss what we can do to go beyond simply identifying wing serial homologs and delve further into the developmental and genetic mechanisms that have facilitated the evolution of insect wings. 2018). 2015; Briscoe and Ragsdale 2018; Kratochwil et al. There is no doubt that insect wing development has been studied most thoroughly in The . 2, Subset of homology assertions used in the present study pertaining to fins, limbs, and related structures. It represents a type of intraorganismal homology, that is, repetitive features (originally) sharing a large proportion of their genetic architecture and developmental pathways (Harris et al. Several leg branches (homologous to a pleural lineage) in the brine shrimp and the crayfish have been shown to express some wing marker genes The results of interest, in this case, would be structures that do not owe their similarity to historical or serial homology, such as fly wings, vertebrate limbs, and beetle horns as appendages, or the light-sensing organs of arthropods, mollusks, and vertebrates as eyes. Thus, implementation of the homology axioms described herein may be useful in providing either a negative or positive filter for search results, depending on the application. Mungall C.J., Gkoutos G.V., Smith C.L., Haendel M.A., Lewis S.E., Ashburner M.. By studying the molecular and developmental mechanisms that orchestrate the differentiation of wing serial homologs from wings (and vice versa), we will be able to identify the mechanisms that are operating uniquely in the winged segments. EntailmentA logical consequence of reasoning across an ontology. notum. However, it is currently unclear how these possible primordial tissues contribute to the formation of wings and wing serial homologs and how these primordia differentiate into very different tissues over the course of development. Homology In: Kampourakis K., editor. Collaboration among various fields, including paleontology and evo-devo, will be fruitful to tackle this century-old question regarding the evolutionary origin of insect wings. Phenoscape: semantic analysis of organismal traits and genes yields insights in evolutionary biology In: Thessen A., editor. 2008; Parmentier et al. et al. This is currently a challenge because of the lack of a standardized reference system for clades in a tree. 2016). Therefore, by identifying various structures that are serially homologous to wings and comparing their development with that of wings, we may be able to reconstruct a transition series from the origin tissue to the wing and therefore identify the key developmental events that led to the acquisition of wings. Renaissance Computing Institute, University of North Carolina, 100 Europa Drive, Suite 540, Chapel Hill, NC 27517, USA, 3 It will be interesting to investigate how much of the gene regulatory network operating in these tissues is shared with insect wings. 2007a. However, in regard to wing serial homologs, the unique dipteran body plan was the problem. The wing and leg marker genes discussed in this review are in the second class of marker genes. 2015), reviews of fin and limb evolution (Hall 2008; Clack 2012), and select papers from the developmental genetic literature (e.g., Shou et al. Further, they do not expect phenotypes to parts of the homologs serial homolog (e.g., humerus of the forelimb), or their developmental precursor (forelimb bud and forelimb wing bud). We explored how to most effectively represent historical and serial homology across anatomical structures to facilitate computational reasoning. Although in many cases, it may suffice for a user to query for serial homologs by using a shared parent term (e.g., a query for vertebra returns vertebra 1, vertebra 2, vertebra 3, etc. Let us first use the legs and their derivatives (ventral appendages) in 2007. The halteres in his flies had wing bristles. Through this outcome, we can conclude that there are no leg serial homologs in the Assertions of homology and statements of lack thereof among the skeletal elements of vertebrates were extracted from the phylogenetic literature on teleost fishes and early sarcopterygians (Dececchi et al. Onthophagus beetles requires the leg gene network for its formation, but it does not transform into the leg upon Hox LOF mutation ap) These expectations are framed from the standpoint of a hypothetical user, a comparative evolutionary anatomist who is well-versed in the data that pertain to homology of the structures under consideration. However, caution must be taken when making this argument, as a developmental process unique to a certain lineage (apomorphic) can superficially mimic possible plesiomorphic conditions. Dorsoventral insect anatomy: The insect thoracic and abdominal body wall can be subdivided into three distinct regions: dorsal (tergum), lateral (pleuron), and ventral (sternum). However, legs were never ectopically induced in the same condition. Serial homology is a special type of homology, defined by Owen as "representative or repetitive relation in the segments of the same organism." [1] Ernst Haeckel preferred the term "homotypy" for the same phenomenon.
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