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      Toward Objective, Morphology-Based Taxonomy: A Case Study on the Malagasy Nesomyrmex sikorai Species Group (Hymenoptera: Formicidae)

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      PLoS ONE

      Public Library of Science

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          Abstract

          Madagascar is one of the world’s greatest biodiversity hotspots, meriting special attention from biodiversity scientists. It is an excellent testing ground for novel techniques in taxonomy that aim to increase classification objectivity and yield greater taxonomic resolving power. Here we reveal the diversity of a unique and largely unexplored fragment of the Malagasy ant fauna using an advanced combination of exploratory analyses on quantitative morphological data allowing for increased objectivity in taxonomic workflow. The diversity of the Nesomyrmex sikorai species-group was assessed via hypothesis-free nest-centroid-clustering combined with recursive partitioning to estimate the number of morphological clusters and determine the most probable boundaries between them. This combination of methods provides a highly automated and objective species delineation protocol based on continuous morphometric data. Delimitations of clusters recognized by these exploratory analyses were tested via confirmatory Linear Discriminant Analysis (LDA) and Multivariate Ratio Analysis (MRA). The final species hypotheses are corroborated by many qualitative characters, and the recognized species exhibit different spatial distributions and occupy different ecological regions. We describe and redescribe eight morphologically distinct species including six new species: Nesomyrmex excelsior sp. n., N. modestus sp. n., N. reticulatus sp. n., N. retusispinosus (Forel, 1892), N. rugosus sp. n., N. sikorai (Emery, 1896), N. striatus sp. n., and N. tamatavensis sp. n. An identification key for their worker castes using morphometric data is provided.

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          Most cited references 15

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          Accelerated modern human–induced species losses: Entering the sixth mass extinction

          Humans are causing a massive animal extinction without precedent in 65 million years.
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            Genome size differentiates co-occurring populations of the planktonic diatom Ditylum brightwellii (Bacillariophyta)

            Background Diatoms are one of the most species-rich groups of eukaryotic microbes known. Diatoms are also the only group of eukaryotic micro-algae with a diplontic life history, suggesting that the ancestral diatom switched to a life history dominated by a duplicated genome. A key mechanism of speciation among diatoms could be a propensity for additional stable genome duplications. Across eukaryotic taxa, genome size is directly correlated to cell size and inversely correlated to physiological rates. Differences in relative genome size, cell size, and acclimated growth rates were analyzed in isolates of the diatom Ditylum brightwellii. Ditylum brightwellii consists of two main populations with identical 18s rDNA sequences; one population is distributed globally at temperate latitudes and the second appears to be localized to the Pacific Northwest coast of the USA. These two populations co-occur within the Puget Sound estuary of WA, USA, although their peak abundances differ depending on local conditions. Results All isolates from the more regionally-localized population (population 2) possessed 1.94 ± 0.74 times the amount of DNA, grew more slowly, and were generally larger than isolates from the more globally distributed population (population 1). The ITS1 sequences, cell sizes, and genome sizes of isolates from New Zealand were the same as population 1 isolates from Puget Sound, but their growth rates were within the range of the slower-growing population 2 isolates. Importantly, the observed genome size difference between isolates from the two populations was stable regardless of time in culture or the changes in cell size that accompany the diatom life history. Conclusions The observed two-fold difference in genome size between the D. brightwellii populations suggests that whole genome duplication occurred within cells of population 1 ultimately giving rise to population 2 cells. The apparent regional localization of population 2 is consistent with a recent divergence between the populations, which are likely cryptic species. Genome size variation is known to occur in other diatom genera; we hypothesize that genome duplication may be an active and important mechanism of genetic and physiological diversification and speciation in diatoms.
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              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.
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                Author and article information

                Affiliations
                Department of Entomology, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA 94118, United States of America
                Universidade de São paulo, BRAZIL
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SC BLF. Performed the experiments: SC. Analyzed the data: SC. Contributed reagents/materials/analysis tools: SC BLF. Wrote the paper: SC BLF.

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                20 April 2016
                2016
                : 11
                : 4
                27097219 4838242 10.1371/journal.pone.0152454 PONE-D-15-43404

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Counts
                Figures: 16, Tables: 1, Pages: 31
                Product
                Funding
                This study was supported by the National Science Foundation under Grant No. DEB-0072713, DEB-0344731, and DEB-0842395 ( http://www.nsf.gov/). SC was supported by the Schlinger Fellowship at the California Academy of Sciences and an Ernst Mayr Travel Grants (Museum of Comparative Zoology, Harvard University), http://www.mcz.harvard.edu/grants_and_funding/ernst-mayr-travel.html. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Research and Analysis Methods
                Imaging Techniques
                Morphometry
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
                Eyes
                Biology and Life Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Eyes
                Research and Analysis Methods
                Mathematical and Statistical Techniques
                Statistical Methods
                Linear Discriminant Analysis
                Physical Sciences
                Mathematics
                Statistics (Mathematics)
                Statistical Methods
                Linear Discriminant Analysis
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Cranium
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Cranium
                Biology and Life Sciences
                Ecology
                Ecosystems
                Forests
                Rainforests
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Forests
                Rainforests
                Ecology and Environmental Sciences
                Terrestrial Environments
                Forests
                Rainforests
                People and Places
                Geographical Locations
                Africa
                Madagascar
                Biology and Life Sciences
                Taxonomy
                Computer and Information Sciences
                Data Management
                Taxonomy
                Biology and Life Sciences
                Taxonomy
                New Species Reports
                Computer and Information Sciences
                Data Management
                Taxonomy
                New Species Reports
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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