István Mikó

Finding Our Way through Phenotypes

Imagine if we could compute across phenotype data as easily as genomic data; this article calls for efforts to realize this vision and discusses the potential benefits.

A Gross Anatomy Ontology for Hymenoptera

Hymenoptera is an extraordinarily diverse lineage, both in terms of species numbers and morphotypes, that includes sawflies, bees, wasps, and ants. These organisms serve critical roles as herbivores, predators, parasitoids, and pollinators, with several species functioning as models for agricultural, behavioral, and genomic research. The collective anatomical knowledge of these insects, however, has been described or referred to by labels derived from numerous, partially overlapping lexicons. The resulting corpus of information—millions of statements about hymenopteran phenotypes—remains inaccessible due to language discrepancies. The Hymenoptera Anatomy Ontology (HAO) was developed to surmount this challenge and to aid future communication related to hymenopteran anatomy. The HAO was built using newly developed interfaces within mx, a Web-based, open source software package, that enables collaborators to simultaneously contribute to an ontology. Over twenty people contributed to the development of this ontology by adding terms, genus differentia, references, images, relationships, and annotations. The database interface returns an Open Biomedical Ontology (OBO) formatted version of the ontology and includes mechanisms for extracting candidate data and for publishing a searchable ontology to the Web. The application tools are subject-agnostic and may be used by others initiating and developing ontologies. The present core HAO data constitute 2,111 concepts, 6,977 terms (labels for concepts), 3,152 relations, 4,361 sensus (links between terms, concepts, and references) and over 6,000 text and graphical annotations. The HAO is rooted with the Common Anatomy Reference Ontology (CARO), in order to facilitate interoperability with and future alignment to other anatomy ontologies, and is available through the OBO Foundry ontology repository and BioPortal. The HAO provides a foundation through which connections between genomic, evolutionary developmental biology, phylogenetic, taxonomic, and morphological research can be actualized. Inherent mechanisms for feedback and content delivery demonstrate the effectiveness of remote, collaborative ontology development and facilitate future refinement of the HAO.

Evolutionary phenomics and the emerging enlightenment of arthropod systematics

Abstract. Published research on the diversity and evolutionary history of Arthropoda sets a high standard for data collection and the integration of novel methods. New phylogenetic estimation algorithms, divergence time approaches, collaborative tools and publishing standards, to name a few, were brought to the broader scientific audience in the context of arthropod systematics. The treatment of morphology in these studies, however, has largely escaped innovation. Lodes rich in characters too often go unexplored, phenotype concepts are published with inadequate documentation and the way observations are textualised leaves them inaccessible to a majority of biologists. We discuss these issues, using data from recent arthropod systematics publications, and offer several that stand to restore the broad utility of morphological data. Specifically, we focus on: (1) the potential of internal soft-part characters and how to integrate their observation into arthropod systematics projects through dissection and serial sectioning; (2) the importance of capturing observations in images, especially using relatively new approaches, like laser scanning confocal microscopy and three-dimensional reconstruction; and (3) the untapped potential of established knowledge representation methods, which may help make the descriptive components of arthropod systematics research more accessible to other domains.

On Dorsal Prothoracic Appendages in Treehoppers (Hemiptera: Membracidae) and the Nature of Morphological Evidence

A spectacular hypothesis was published recently, which suggested that the “helmet” (a dorsal thoracic sclerite that obscures most of the body) of treehoppers (Insecta: Hemiptera: Membracidae) is connected to the 1st thoracic segment (T1; prothorax) via a jointed articulation and therefore was a true appendage. Furthermore, the “helmet” was interpreted to share multiple characteristics with wings, which in extant pterygote insects are present only on the 2nd (T2) and 3rd (T3) thoracic segments. In this context, the “helmet” could be considered an evolutionary novelty. Although multiple lines of morphological evidence putatively supported the “helmet”-wing homology, the relationship of the “helmet” to other thoracic sclerites and muscles remained unclear. Our observations of exemplar thoraces of 10 hemipteran families reveal multiple misinterpretations relevant to the “helmet”-wing homology hypothesis as originally conceived: 1) the “helmet” actually represents T1 (excluding the fore legs); 2) the “T1 tergum” is actually the anterior dorsal area of T2; 3) the putative articulation between the “helmet” and T1 is actually the articulation between T1 and T2. We conclude that there is no dorsal, articulated appendage on the membracid T1. Although the posterior, flattened, cuticular evagination (PFE) of the membracid T1 does share structural and genetic attributes with wings, the PFE is actually widely distributed across Hemiptera. Hence, the presence of this structure in Membracidae is not an evolutionary novelty for this clade. We discuss this new interpretation of the membracid T1 and the challenges of interpreting and representing morphological data more broadly. We acknowledge that the lack of data standards for morphology is a contributing factor to misinterpreted results and offer an example for how one can reduce ambiguity in morphology by referencing anatomical concepts in published ontologies.

Folding wings like a cockroach: A review of transverse wing folding ensign wasps (Hymenoptera: Evaniidae: Afrevania and Trissevania)

We revise two relatively rare ensign wasp genera, whose species are restricted to Sub-Saharan Africa: Afrevania and Trissevania. Afrevania longipetiolata sp. nov., Trissevania heatherae sp. nov., T. hugoi sp. nov., T. mrimaensis sp. nov. and T. slideri sp. nov. are described, males and females of T. anemotis and Afrevania leroyi are redescribed, and an identification key for Trissevaniini is provided. We argue that Trissevania mrimaensis sp. nov. and T. heatherae sp. nov. populations are vulnerable, given their limited distributions and threats from mining activities in Kenya. We hypothesize that these taxa together comprise a monophyletic lineage, Trissevaniini, tr. nov., the members of which share the ability to fold their fore wings along two intersecting fold lines. Although wing folding of this type has been described for the hind wing of some insects four-plane wing folding of the fore wing has never been documented. The wing folding mechanism and the pattern of wing folds of Trissevaniini is shared only with some cockroach species (Blattodea). It is an interesting coincidence that all evaniids are predators of cockroach eggs. The major wing fold lines of Trissevaniini likely are not homologous to any known longitudinal anatomical structures on the wings of other Evaniidae. Members of the new tribe share the presence of a coupling mechanism between the fore wing and the mesosoma that is composed of a setal patch on the mesosoma and the retinaculum of the fore wing. While the setal patch is an evolutionary novelty, the retinaculum, which originally evolved to facilitate fore and hind wing coupling in Hymenoptera, exemplifies morphological exaptation. We also refine and clarify the Semantic Phenotype approach used in previous taxonomic revisions and explore the consequences of merging new with existing data. The way that semantic statements are formulated can evolve in parallel, alongside improvements to the ontologies themselves.

Systematic re-appraisal of the gall-usurping wasp genus Synophrus Hartig, 1843 (Hymenoptera: Cynipidae: Synergini).

Several unanswered questions remain regarding the taxonomy and phylogeny of inquiline gallwasps (Cynipidae: Synergini), obligate inhabitants of plant galls induced primarily by other gallwasps (Cynipidae: Cynipini and Diplolepidini). Here we use morphological and molecular data to revise the inquiline genus Synophrus, members of which are notable for extensively modifying the structure of galls induced by oak gallwasp hosts on oaks in the section Cerris of Quercus subgenus Quercus in the Western Palaearctic. Previous taxonomic treatments have recognized three Western Palaearctic species of Synophrus: S. pilulae, S. politus and S. olivieri. Our results support the establishment of four additional Western Palaearctic species: Synophrus hungaricussp.n., S. libanisp.n., S. syriacussp.n. and S. hispanicussp.n. We describe and diagnose these new taxa, analyse their phylogenetic relationships, and show that Synophrus inquilines are able to impose their own gall phenotypes on those of their hosts. We provide an updated key to Synophrus.

Male terminalia of Ceraphronoidea: morphological diversity in an otherwise monotonous taxon

The skeletomuscular system of male terminalia in Evaniomorpha (Hymenoptera) is described and the functional morphology of male genitalia is discussed. Confocal laser scanning microscopy is the primary method used for illustrating anatomical phenotypes, and a domain-specific anatomy ontology is employed to more explicitly describe anatomical structures. A comprehensive data set of ceraphronoid male genitalia is analyzed, yielding the first phylogeny of the superfamily. One hundred and one taxa, including three outgroups, are scored for 48 characters. Ceraphronoidea are recovered as sister to the remaining Evaniomorpha in the implied weighting analyses. Numerous character states suggest that Ceraphronoidea is a relatively basal apocritan lineage. Ceraphronoidea, Ceraphronidae, and Megaspilinae are each retrieved as monophyletic in all analyses. Megaspilidae is not recovered as monophyletic. Lagynodinae is monophyletic in the implied weighting analyses with strong support and is a polytomy in the equal weighting analysis. Lagynodinae shares numerous plesiomorphies with both Megaspilinae and Ceraphronidae. Relationships among genera are weakly corroborated. Masner is sister of Ceraphronidae. Trassedia is nested within Ceraphronidae based on the present analysis. Because of this and numerous features shared between it and Ceraphron we transfer Trassedia from Megaspilidae to Ceraphronidae. Dendrocerus forms a single monophyletic clade, with modest support, together with some Conostigmus species. This result challenges the utility of such traditional diagnostic characters as ocellar arrangement and shape of the male flagellomeres. Aphanogmus is monophyletic in the implied weighting, but remains a polytomy with Ceraphron in the equal weighting analysis. Gnathoceraphron is always nested within a well-supported Aphanogmus clade. Cyoceraphron and Elysoceraphron are nested within Ceraphron and Aphanogmus, respectively. The male genitalia prove to be a substantial source of phylogenetically relevant information. Our results indicate that a reclassification of Ceraphronoidea both at the family and generic level is necessary but that more data are required.

New neotropical species of Opiinae (Hymenoptera, Braconidae) reared from fruit-infesting and leaf-mining Tephritidae (Diptera) with comments on the Diachasmimorpha mexicana species group and the genera Lorenzopius and Tubiformopius

Abstract Four new species of opiine Braconidae are described from Mexico. These are Diachasmimorpha martinalujai Wharton reared from Rhagoletis infesting fruits of Crataegus spp., Diachasmimorpha norrbomi Wharton reared from Euphranta mexicana infesting fruits of Ribes pringlei, Eurytenes (Stigmatopoea) norrbomi Wharton reared from Trypeta concolor mining leaves of Barkleyanthus salicifolia and Eurytenes (Stigmatopoea) maya Wharton reared from Rhagoletis pomonella infesting apples and fruits of Crataegus spp. Morphological features of the first metasomal segment and occipital carina, useful for placement of these species, are discussed relative to the genera Diachasmimorpha, Eurytenes, Lorenzopius, Tubiformopius, and Opius s.l. Descriptions and diagnoses are referenced to the Hymenoptera Anatomy Ontology. The following represent new combinations: Diachasmimorpha hildagensis, Lorenzopius euryteniformis, and Tubiformopius tubibasis. Revised diagnoses are provided for Diachasmimorpha hildagensis, Diachasmimorpha mexicana, Diachasmimorpha sanguinea, Eurytenes (Stigmatopoea), Lorenzopius, Lorenzopius euryteniformis, Tubiformopius, Tubiformopius tubigaster, Tubiformopius tubibasis, Opius incoligma, and Opius rugicoxis. Two species groups are delineated within Lorenzopius and a key to species of Diachasmimorpha occurring in the New World is provided.

Taxonomic Synopsis of the Ponto-Mediterranean Ants of Temnothorax nylanderi Species-Group.

In the current revisionary work, the Temnothorax nylanderi species-group of myrmicine ants is characterized. Eighteen species belonging to this group in the Ponto-Mediterranean region are described or redefined based on an integrative approach that combines exploratory analyses of morphometric data and of a 658bp fragment of the mitochondrial gene for the cytochrome c oxidase subunit I (CO I). The species group is subdivided into five species complexes: T. angustifrons complex, T. lichtensteini complex, T. nylanderi complex, T. parvulus complex, T. sordidulus complex, and two species, T. angulinodis sp. n. and T. flavicornis (Emery, 1870) form their own lineages. We describe seven new species (T. angulinodis sp. n., T. angustifrons sp. n., T. ariadnae sp. n., T. helenae sp. n., T. lucidus sp. n., T. similis sp. n., T. subtilis sp. n.), raise T. tergestinus (FINZI, 1928) stat.n. to species level, and propose a new junior synonymy for T. saxonicus (SEIFERT, 1995) syn.n. (junior synonym of T. tergestinus). We describe the worker caste and provide high quality images and distributional maps for all eighteen species. Furthermore, we provide a decision tree as an alternative identification key that visually gives an overview of this species-group. We make the first application to Formicidae of the Semantic Phenotype approach that has been used in previous taxonomic revisions.

Matching arthropod anatomy ontologies to the Hymenoptera Anatomy Ontology: results from a manual alignment

Matching is an important step for increasing interoperability between heterogeneous ontologies. Here, we present alignments we produced as domain experts, using a manual mapping process, between the Hymenoptera Anatomy Ontology and other existing arthropod anatomy ontologies (representing spiders, ticks, mosquitoes and Drosophila melanogaster). The resulting alignments contain from 43 to 368 mappings (correspondences), all derived from domain-expert input. Despite the many pairwise correspondences, only 11 correspondences were found in common between all ontologies, suggesting either major intrinsic differences between each ontology or gaps in representing each group’s anatomy. Furthermore, we compare our findings with putative correspondences from Bioportal (derived from LOOM software) and summarize the results in a total evidence alignment. We briefly discuss characteristics of the ontologies and issues with the matching process. Database URL: http://purl.obolibrary.org/obo/hao/2012-07-18/arthropod-mappings.obo