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Type: Article
Published: 2016-01-22
Page range: 361–372
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Antennal sensory organs of Scathophaga stercoraria (Linnaeus, 1758) (Diptera: Scathophagidae): ultramorphology and phylogenetic implications

School of Nature Conservation, Beijing Forestry University, Qinghua East Road No. 35, Beijing 100083, China
School of Nature Conservation, Beijing Forestry University, Qinghua East Road No. 35, Beijing 100083, China
School of Nature Conservation, Beijing Forestry University, Qinghua East Road No. 35, Beijing 100083, China
School of Nature Conservation, Beijing Forestry University, Qinghua East Road No. 35, Beijing 100083, China
Diptera Scathophaga stercoraria antenna sensilla setiferous plaques scanning electron microscopy phylogeny

Abstract

Scathophaga stercoraria (Linnaeus, 1758) is a well-established insect model species involved in numerous investigations on behavior, biology, phylogeny, genetics and evolution. The antennal sensilla of S. stercoraria are examined via scanning electron microscopy in order to emphasize their importance on taxonomy and phylogeny. On antennal scape and pedicel, both microtrichiae and several sharp-tipped mechanoreceptors are observed, while another two structures, setiferous plaques and pedicellar button, are also detected on antennal pedicel. One type of sensory pit and four types of antennal sensilla, including trichoid sensilla, basiconic sensilla, coeloconic sensilla and clavate sensilla, are observed on antennal funiculus. Similarity and disparity of setiferous plaques among different calyptrate groups are analyzed in terms of phylogeny. The phylogenetic results supported by morphology of setiferous plaques strongly accord with the cladistic relations based on known molecular tree, implying the potential taxonomic and phylogenetic implications of the plaques in Calyptratae.

 

References

  1. Amer, A. & Mehlhorn, H. (2006) The sensilla of Aedes and Anopheles mosquitoes and their importance in repellency. Parasitology Research, 99, 491–499.
    http://dx.doi.org/10.1007/s00436-006-0185-0

    Bernasconi, M.V., Valsangiacomo, C., Piffaretti, J.C. & Ward, P.I. (2000) Phylogenetic relationships among Muscoidea (Diptera: Calyptratae) based on mitochondrial DNA sequences. Insect Molecular Biology, 9, 67–74.|
    http://dx.doi.org/10.1046/j.1365-2583.2000.00158.x

    Blanckenhorn, W.U. (1998a) Adaptive phenotypic plasticity in growth rate and diapause in the yellow dung fly. Evolution, 52, 1394–1407.
    http://dx.doi.org/10.2307/2411309

    Blanckenhorn, W.U. (1998b.) Altitudinal differentiation in diapause response in two species of dung flies. Ecological Entomology, 23, 1–8.
    http://dx.doi.org/10.1046/j.1365-2311.1998.00098.x

    Blanckenhorn, W.U. & Viele S.N.T. (1999) Foraging in yellow dung flies: testing for a small-male time budget advantage. Ecological Entomology, 24, 1–6.
    http://dx.doi.org/10.1046/j.1365-2311.1999.00171.x

    Blanckenhorn, W.U. (2002) The consistency of heritability estimates in field and laboratory in the yellow dung fly. Genetica, 114, 171–182.
    http://dx.doi.org/10.1023/A:1015181516827

    Blanckenhorn, W.U. & Llaurens, V. (2005) Effects of temperature on cell size and number in the yellow dung fly Scathophaga stercoraria. Journal of Thermal Biology, 30, 213–219.
    http://dx.doi.org/10.1016/j.jtherbio.2004.11.004

    Dittmar, K., Porter, M.L., Murray, S. & Whiting, M.F. (2006) Molecular phylogenetic analysis of nycteribiid and streblid bat flies (Diptera: Brachycera, Calyptratae): Implications for host associations and phylogeographic origins. Molecular Phylogenetics and Evolution, 38, 155–170.
    http://dx.doi.org/10.1016/j.ympev.2005.06.008

    Faucheux, M.J. & Mason, F. (2000a) Les antennes des Némotélinés (Insecta: Diptera: Stratiomyidae). I: Nemotelus Geoffroy et Cluninemotelus Mason. Bulletin de la Société des Sciences Naturelles de l’Ouest de la France, New Series, 22, 49–70.

    Faucheux, M.J. & Mason, F. (2000b) Les antennes des Némotélinés (Insecta: Diptera: Stratiomyidae). II: Les organes sensoriels de Pselaphomyia nigripennis (Bigot). Bulletin de la Société des Sciences Naturelles de l’Ouest de la France, New Series, 22, 139–150.

    Faucheux, M.J. & Mason, F. (2000c) Les antennes des Némotélinés. III: Lasiopa Brullé, Epideicticus Kertész, Brachycera Thomson. Comparaison avec les Béridinés: Beris Latreille (Insecta: Diptera: Stratiomyidae). Bulletin de la Société des Sciences Naturelles de l’Ouest de la France (n.s.), 22, 186–204.

    Fernandes, F. de F., Pimenta, P.F.P., & Linardi, P.M. (2004). Antennal sensilla of the new world screwworm fly, Cochliomyia hominivorax (Diptera: Calliphoridae). Journal of Medical Entomology, 41, 545–551.
    http://dx.doi.org/10.1603/0022-2585-41.4.545

    Fernandes, F.F., Freitas, E.P.S., Linardi, P.M. & Pimenta, P.F.P. (2005) Ultrastructure of contact-chemoreceptor sensilla found among the genae of female Gasterophilus nasalis. Journal of Parasitology, 91, 1218–1220.
    http://dx.doi.org/10.1645/GE-501R3.1

    Floate, K.D. (1998) Off-target effects of ivermectin on insects and on dung degradation in southern Alberta, Canada. Bulletin of Entomological Research, 88, 25–35.
    http://dx.doi.org/10.1017/S0007485300041523

    Floate, K.D. (2007) Endectocide residues affect insect attraction to dung from treated cattle: Implications for toxicity tests. Medical and Veterinary Entomology, 21, 312–322.
    http://dx.doi.org/10.1111/j.1365-2915.2007.00702.x

    Floate, K.D. & Coghlin, P.C. (2010) No support for fluctuating asymmetry as a biomarker of chemical residues in livestock dung. Canadian Entomologist, 142, 354–368.
    http://dx.doi.org/10.4039/n10-014

    Greenberg, B. (1970) Species distribution of new structures on fly antennae. Nature, 228, 1338–1339.
    http://dx.doi.org/10.1038/2281338a0

    Greenberg, B. & Ash, N. (1972) Setiferous plaques on antennal pedicels of Muscoid Diptera: Appearance in various species and tests of function. Annals of the Entomological Society of America, 65, 1340–1346.
    http://dx.doi.org/10.1093/aesa/65.6.1340

    Hosken, D.J. & Ward, P.I. (1999) Female accessory reproductive gland activity in the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae). Journal of Insect Physiology, 45, 809–814.
    http://dx.doi.org/10.1016/S0022-1910(98)00159-0

    Hosken, D.J., Blanckenhorn, W.U. & Ward, P.I. (2000) Developmental stability in yellow dung flies (Scathophaga stercoraria): Fluctuating asymmetry, heterozygosity and environmental stress. Journal of Evolutionary Biology, 13, 919–926.
    http://dx.doi.org/10.1046/j.1420-9101.2000.00239.x

    Hosken, D.J., Garner, T.W.J. & Ward, P.I. (2001) Sexual conflict selects for male and female reproductive characters. Current Biology, 11, 489–493.
    http://dx.doi.org/10.1016/S0960-9822(01)00146-4

    Hunter, F.F. & Adserballe, C.F. (1996) Cuticular structures on the antennae of Hypoderma bovis De Geer (Diptera: Oestridae) females. International Journal of Insect Morphology and Embryology, 25, 173–181.
    http://dx.doi.org/10.1016/0020-7322(95)00013-5

    Kraushaar, U., Goudet, J. & Blanckenhorn, W.U. (2002) Geographical and altitudinal population genetic structure of two dung fly species with contrasting mobility and temperature preference. Heredity, 89, 99–106.
    http://dx.doi.org/10.1038/sj.hdy.6800097

    Kutty, S.N., Pape, T., Pont, A., Wiegmann, B.M. & Meier, R. (2008) The Muscoidea (Diptera: Calyptratae) are paraphyletic: Evidence from four mitochondrial and four nuclear genes. Molecular Phylogenetics and Evolution, 49, 639–652.
    http://dx.doi.org/10.1016/j.ympev.2008.08.012

    Kutty, S.N., Pape, T., Wiegmann, B.M. & Meier, R. (2010) Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidea and the position of Mystacinobiidae and McAlpine’s fly. Systematic Entomology, 35, 614–635.
    http://dx.doi.org/10.1111/j.1365-3113.2010.00536.x

    Liu, X.H., Zhang, M., Shi, J.N., Li, K. & Zhang, D. (2013) Ultrastructure of antennal sensilla of a parasitoid fly, Pales pavida Meigen (Diptera: Tachinidae). Micron, 54, 36–42.
    http://dx.doi.org/10.1016/j.micron.2013.08.002

    Marshall, A.T. & Lewis, C.T. (1971) Structural variation in the antennal sense organs of fulgoroid Homoptera (Insecta). Zoological Journal of the Linnean Society, 50, 181–184.
    http://dx.doi.org/10.1111/j.1096-3642.1971.tb00758.x

    Nirmala, X., Hypsa, V. & Zurovec, M. (2001) Molecular phylogeny of Calyptratae (Diptera: Brachycera): the evolution of 18S and 16S ribosomal rDNAs in higher dipterans and their use in phylogenetic inference. Insect Molecular Biology, 10, 475–485.
    http://dx.doi.org/10.1046/j.0962-1075.2001.00286.x

    Parker, G.A. (1970a) The reproductive behaviour and the nature of sexual selection in Scathophaga stercoraria L. (Diptera: Scathophagidae) I. Diurnal and seasonal changes in population density around the site of mating and oviposition. Journal of Animal Ecology, 39, 185–204.
    http://dx.doi.org/10.2307/2895

    Parker, G.A. (1970b) The reproductive behaviour and the nature of sexual selection in Scathophaga stercoraria L. (Diptera: Scathophagidae). II. The fertilization rate and the spatial and temporal relationships of each sex around the site of mating and oviposition. Journal of Animal Ecology, 39, 205–228.
    http://dx.doi.org/10.2307/2896

    Parker, G.A. (1970c) Sperm competition and its evolutionary effect on copula duration in the fly Scathophaga stercoraria. Journal of Insect Physiology, 16, 1301–1328.
    http://dx.doi.org/10.1016/0022-1910(70)90131-9

    Parker, G.A. (1978) Searching for mates. In: Krebs, J.R. & Davies, N.B. (Eds.), Behavioural Ecology. The Wiley-Blackwell Press, Oxford, pp. 214–244.

    Petersen, F.T., Meier, R., Kutty, S.N. & Wiegmann, B.M. (2007) The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Molecular Phylogenetics and Evolution, 45, 111–122.
    http://dx.doi.org/10.1016/j.ympev.2007.04.023

    Poddighe, S., Dekker, T., Scala, A. & Angioy A.M. (2010) Olfaction in the female sheep botfly. Naturwissenschaften, 97, 827–835.
    http://dx.doi.org/10.1007/s00114-010-0700-0

    Rahal, Y., Barry, P., Hawlitzky, N. & Renou, M. (1996) Antennal olfactory sensilla of the parasitoid fly, Pseudoperichaeta nigrolineata Walker (Diptera: Tachinidae). International Journal of Insect Morphology and Embryology, 25, 145–152.
    http://dx.doi.org/10.1016/0020-7322(95)00026-7

    Reim, C., Teuschl, Y. & Blanckenhorn, W.U. (2006) Size-dependent effects of larval and adult food availability on reproductive energy allocation in the yellow dung fly. Functional Ecology, 20, 1012–1021.
    http://dx.doi.org/10.1111/j.1365-2435.2006.01173.x

    Römbke, J., Barrett, K., Gray, J., Blanckenhorn, W.U., Jochmann, R., Knäbe, S., Lehmhus, J., Rosenkranz, B., Sekine, T., Scheffczyk, A., Schmidt, T., Sharples, A. & Davies, N. (2009) Lethal and sublethaltoxic effects of a test chemical (ivemectin) on the Yellow Dung Fly Scathophaga stercoraria based on a standardsized international ring test. Environmental Toxicology & Chemistry, 28, 2117–2124.
    http://dx.doi.org/10.1897/08-599.1

    Ross, K.T.A. (1992) Comparative study of the antennal sensilla of five species of root maggots: Delia radicum L., D. floralis F., D. antique MG, D. platura MG. (Diptera: Anthomyiidae), and Psila rosae F. (Diptera: Psilidae). International Journal of Insect Morphology and Embryology, 21, 175–197.
    http://dx.doi.org/10.1016/0020-7322(92)90015-F

    Scotland, R.W., Olmstead, R.G. & Bennett, J.R. (2003) Phylogeny reconstruction: the role of morphology. Systematic Biology, 52, 539–548.
    http://dx.doi.org/10.1080/10635150390223613

    Setzu, M.D., Poddighe, S. & Angioy, A.M. (2011) Sensilla on the antennal funiculus of the blow fly, Protophormia terraenovae (Diptera: Calliphoridae). Micron, 42, 471–477.
    http://dx.doi.org/10.1016/j.micron.2011.01.005

    Smallegange, R.C., Kelling, R.J. & Otter, C.J. (2008) Types and numbers of sensilla on antennae and maxillary palps of small and large houseflies, Musca domestica (Diptera, Muscidae). Microscopy Research and Technique, 71, 880–886.
    http://dx.doi.org/10.1002/jemt.20636

    Sommer, C., Steffansen, B., Overgaard Nielsen, B., Gronvold, J., Vagn-Jensen, K.M., Brochner, J., Jespersen, J., Springborg, J. & Nansen, P. (1992) Ivermectin excreted in cattle dung after subcutaneous injection or pour-on treatment: Concentrations and impact on dung fauna. Bulletin of Entomological Research, 82, 257–264.
    http://dx.doi.org/10.1017/S0007485300051804

    Strong, L. & James, S. (1992) Some effects of rearing the yellow dung fly Scathophaga stercoraria in cattle dung containing Ivermectin. Entomologia Experimentalis et Applicata, 63, 39–45.
    http://dx.doi.org/10.1111/j.1570-7458.1992.tb02417.x

    Sukontason, K., Sukontason, K.L., Piangjai, S., Boonchu, N., Chaiwong, T., Ngern-klun, R., Sripakdee, D., Vogtsberger, R.C. & Olson, J.K. (2004) Antennal sensilla of some forensically important flies in families Calliphoridae, Sarcophagidae and Muscidae. Micron, 35, 671–679.
    http://dx.doi.org/10.1016/j.micron.2004.05.005

    Sukontason, K., Methanitikorn, R., Chaiwong, T., Kurahashi, H., Vogtsberger, R.C. & Sukontason, K.L. (2007) Sensilla of the antenna and palp of Hydrotaea chalcogaster (Diptera: Muscidae). Micron, 38, 218–223.
    http://dx.doi.org/10.1016/j.micron.2006.07.018

    Swaddle, J.P. (1997) Developmental stability and predation success in an insect predator prey system. Behavioral Ecology, 8, 433–436.
    http://dx.doi.org/10.1093/beheco/8.4.433

    Teuschl, Y., Reim, C. & Blanckenhorn, W.U. (2007) Correlated responses to artificial body size selection in growth, development, phenotypic plasticity and juvenile viability in yellow dung flies. Journal of Evolutionary Biology, 20, 87–103.
    http://dx.doi.org/10.1111/j.1420-9101.2006.01225.x

    Urbanek, A., Piotrowicz, M., Szadziewski, R. & Gilka, W. (2014) Sensilla coeloconica ringed by microtrichia in host-seeking biting midges. Medical and veterinary entomology, 28, 355–363.
    http://dx.doi.org/10.1111/mve.12057

    Wang, Q.K., Zhang, M., Li, K. & Zhang, D. (2012) Olfactory sensilla on antennae and maxillary palps of Fannia hirticeps (Stein, 1892) (Diptera: Fanniidae). Microscopy Research and Technique, 75, 1313–1320.
    http://dx.doi.org/10.1002/jemt.22066

    Wang, Q.K., Yang, Y.Z., Liu, M.Q. & Zhang, D. (2014a) Fine structure of Delia platura (Meigen) (Diptera: Anthomyiidae) revealed by scanning electron microscopy. Microscopy research and technique, 77, 619–630.
    http://dx.doi.org/10.1002/jemt.22380

    Wang, Q.K., Liu, X.H., Lu, P.F. & Zhang, D. (2014b) Ultrastructure of antennal sensilla in Hydrotaea armipes (Fallén) (Diptera: Muscidae): New evidence for taxonomy of the genus Hydrotaea. Zootaxa, 3790 (4), 577–586.
    http://dx.doi.org/10.11646/zootaxa.3790.4.6

    Ward, P.I. (2000) Cryptic female choice in the yellow dung fly Scathophaga stercoraria. Evolution, 54, 1680–1686.
    http://dx.doi.org/10.1554/0014-3820(2000)054[1680:CFCITY]2.0.CO;2

    Ward, P.I. (2007) Postcopulatory selection in the yellow dung fly Scathophaga stercoraria (L.) and the mate-now-choose-later mechanism of cryptic female choice. Advances in the Study of Behavior, 37, 343–370.
    http://dx.doi.org/10.1016/S0065-3454(07)37007-1

    Webb, L., Beaumont, D.J., Nager, R.G. & McCracken, D.I. (2007) Effects of avermectin residues in cattle dung on yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae) populations in grazed pastures. Bulletin of Entomological Research, 97, 129–138.
    http://dx.doi.org/10.1017/S0007485307004683

    Wiegmann, B.M., Trautwein, M.D., Winkler, I.S., Barr, N.B., Kim, J.W., Lambkin, C., Bertone, M.A., Cassel, B.K., Bayless, K.M., Heimberg, A.M., Wheeler, B.M., Peterson, K.J., Pape T., Sinclair, B.J., Skevington, J.H., Blagoderov, V., Caravas, J, Kutty, S.N., Schmidt-Ott, U., Kampmeier, G.E., Thompson, F.C., Grimaldi, D.A., Beckenbach, A.T., Courtney, G.W., Friedrich, M., Meier, R. & Yeates, D.K. (2011) Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences, 108, 5690–5695.
    http://dx.doi.org/10.1073/pnas.1012675108

    Yeates, D.K. & Wiegmann, B.M. (2005) Phylogeny and evolution of Diptera: recent insights and new perspectives. In: Yeates, D.K. & Wiegmann, B.M. (Eds), The evolutionary biology of flies. Columbia University Press, New York, pp. 14–44.

    Zhang, D., Wang, Q.K., Hu, D.F. & Li, K. (2012a) Sensilla on the antennal funiculus of the horse stomach bot fly, Gasterophilus nigricornis. Medical and Veterinary Entomology, 26, 314–322.
    http://dx.doi.org/10.1111/j.1365-2915.2011.01007.x

    Zhang, D., Wang, Q.K., Hu, D.F. & Li, K. (2012b) Cuticular structures on antennae of the bot fly, Portschinskia magnifica (Diptera: Oestridae). Parasitology Research, 111, 1651–1659.
    http://dx.doi.org/10.1007/s00436-012-3004-9

    Zhang, D., Wang, Q.K., Yang, Y.Z., Chen, Y.O. & Li, K. (2013a) Sensory organs of the antenna of two medically and hygienically important Fannia species (Diptera: Fanniidae). Parasitology Research, 112, 2177–2185.
    http://dx.doi.org/10.1007/s00436-013-3377-4

    Zhang, D., Liu, X.H., Li, X.Y., Zhang, M. & Li, K. (2013b) Antennal sensilla of the green bottle fly, Lucilia sericata (Meigen) (Diptera: Calliphoridae). Parasitology Research, 112, 3843–3850.
    http://dx.doi.org/10.1007/s00436-013-3573-2

    Zhang, D., Wang, Q.K., Liu, X.H. & Li, K. (2013c) Sensilla on antenna and maxillary palp of predaceous fly, Lispe neimongola Tian et Ma (Diptera: Muscidae). Micron, 49, 33–39.
    http://dx.doi.org/10.1016/j.micron.2013.02.012

    Zhang, D., Liu, X.H., Li, X.Y., Cao, J., Chu, H.J. & Li, K. (2015) Ultrastructural investigation of antennae in three cutaneous myiasis flies: Melophagus ovinus, Hippobosca equina, and Hippobosca longipennis (Diptera: Hippoboscidae). Parasitology Research, 114, 1887–1896.
    http://dx.doi.org/ 10.1007/s00436-015-4376-4