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      Long Frontal Projections Help Battus philenor (Lepidoptera: Papilionidae) Larvae Find Host Plants

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          Abstract

          Animals sometimes develop conspicuous projections on or near their heads as, e.g., weaponry, burrowing or digging tools, and probes to search for resources. The frontal projections that insects generally use to locate and assess resources are segmented appendages, including antennae, maxillary palps, and labial palps. There is no evidence to date that arthropods, including insects, use projections other than true segmental appendages to locate food. In this regard, it is noteworthy that some butterfly larvae possess a pair of long antenna-like projections on or near their heads. To date, the function of these projections has not been established. Larvae of pipevine swallowtail butterflies Battus philenor (Papilionidae) have a pair of long frontal fleshy projections that, like insect antennae generally, can be actively moved. In this study, we evaluated the possible function of this pair of long moveable frontal projections. In laboratory assays, both frontal projections and lateral ocelli were shown to increase the frequency with which search larvae found plants. The frontal projections increased finding of host and non-host plants equally, suggesting that frontal projections do not detect host-specific chemical cues. Detailed SEM study showed that putative mechanosensillae are distributed all around the frontal as well as other projections. Taken together, our findings suggest that the frontal projections and associated mechanosensillae act as vertical object detectors to obtain tactile information that, together with visual information from lateral ocelli and presumably chemical information from antennae and mouthparts, help larvae to find host plants. Field observations indicate that host plants are small and scattered in southern Arizona locations. Larvae must therefore find multiple host plants to complete development and face significant challenges in doing so. The frontal projections may thus be an adaptation for finding a scarce resource before starving to death. This is the first evidence that arthropods use projections other than true segmental appendages such as antennae, mouthparts and legs, to locate food resources.

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          Most cited references20

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          The organization of the chemosensory system in Drosophila melanogaster: a review.

          R Stocker (1994)
          This review surveys the organization of the olfactory and gustatory systems in the imago and in the larva of Drosophila melanogaster, both at the sensory and the central level. Olfactory epithelia of the adult are located primarily on the third antennal segment (funiculus) and on the maxillary palps. About 200 basiconic (BS), 150 trichoid (TS) and 60 coeloconic sensilla (CS) cover the surface of the funiculus, and an additional 60 BS are located on the maxillary palps. Males possess about 30% more TS but 20% fewer BS than females. All these sensilla are multineuronal; they may be purely olfactory or multimodal with an olfactory component. Antennal and maxillary afferents converge onto approximately 35 glomeruli within the antennal lobe. These projections obey precise rules: individual fibers are glomerulus-specific, and different types of sensilla are associated with particular subsets of glomeruli. Possible functions of antennal glomeruli are discussed. In contrast to olfactory sensilla, gustatory sensilla of the imago are located at many sites, including the labellum, the pharynx, the legs, the wing margin and the female genitalia. Each of these sensory sites has its own central target. Taste sensilla are usually composed of one mechano- and three chemosensory neurons. Individual chemosensory neurons within a sensillum respond to distinct subsets of molecules and project into different central target regions. The chemosensory system of the larva is much simpler and consists essentially of three major sensillar complexes on the cephalic lobe, the dorsal, terminal and ventral organs, and a series of pharyngeal sensilla.
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            Condition-dependent signalling of genetic variation in stalk-eyed flies.

            Handicap models of sexual selection predict that male sexual ornaments have strong condition-dependent expression and this allows females to evaluate male genetic quality. A number of previous experiments have demonstrated heightened condition-dependence of sexual ornaments in response to environmental stress. Here we show that genetic variation underlies the response to environmental stress (variable food quality) of a sexual ornament (male eye span) in the stalk-eyed fly Cyrtodiopsis dalmanni. Some male genotypes develop large eye span under all conditions, whereas other genotypes progressively reduce eye span as conditions deteriorate. Several non-sexual traits (female eye span, male and female wing length) also show genetic variation in condition-dependent expression, but their genetic response is entirely explained by scaling with body size. In contrast, the male sexual ornament still reveals genetic variation in the response to environmental stress after accounting for differences in body size. These results strongly support the hypothesis that female mate choice yields genetic benefits for offspring.
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              Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae).

              Both ornaments and weapons of sexual selection frequently exhibit prolific interspecific diversity of form. Yet, most studies of this diversity have focused on ornaments involved with female mate choice, rather than on the weapons of male competition. With few exceptions, the mechanisms of divergence in weapon morphology remain largely unexplored. Here, we characterize the evolutionary radiation of one type of weapon: beetle horns. We use partial sequences from four nuclear and three mitochondrial genes to develop a phylogenetic hypothesis for a worldwide sample of 48 species from the dung beetle genus Onthophagus (Coleoptera: Scarabaeidae). We then use these data to test for multiple evolutionary origins of horns and to characterize the evolutionary radiation of horns. Although our limited sampling of one of the world's most species-rich genera almost certainly underestimates the number of evolutionary events, our phylogeny reveals prolific evolutionary lability of these exaggerated sexually selected weapons (more than 25 separate gains and losses of five different horn types). We discuss these results in the context of the natural history of these beetles and explore ways that sexual selection and ecology may have interacted to generate this extraordinary diversity of weapon morphology.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                29 July 2015
                2015
                : 10
                : 7
                : e0131596
                Affiliations
                [1 ]Laboratory of Entomology, Faculty of Agriculture, Kinki University, Nara, Japan
                [2 ]Forestry and Forest Products Research Institute, Tsukuba, Japan
                [3 ]Department of Integrative Biology, University of California, Berkeley, United States of America
                [4 ]Laboratory of Conservation Ecology, Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
                [5 ]Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, United States of America
                Institute of Plant Physiology and Ecology, CHINA
                Author notes

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

                Conceived and designed the experiments: IK DRP. Performed the experiments: IK KT. Analyzed the data: IK. Contributed reagents/materials/analysis tools: TY TAS. Wrote the paper: IK DRP KT. Comment and advice: TY.

                Article
                PONE-D-15-03159
                10.1371/journal.pone.0131596
                4519131
                26222554
                db834699-2932-433b-b352-879dcdc178fe
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 22 January 2015
                : 3 June 2015
                Page count
                Figures: 8, Tables: 2, Pages: 18
                Funding
                The authors have no support or funding to report.
                Categories
                Research Article
                Custom metadata
                All relevant data are available in the manuscript and its Supporting Information files.

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