Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-22T12:14:15.589Z Has data issue: false hasContentIssue false
  • English
  • Français

The relationship between asymmetry, size and unusual venation in honey bees (Apis mellifera)

Published online by Cambridge University Press:  04 March 2016

S. Łopuch  and
A. Tofilski
S. Łopuch*
Affiliation:
Department of Pomology and Apiculture, Agricultural University, 29 Listopada 54, 31-425 Krakow, Poland
A. Tofilski
Affiliation:
Department of Pomology and Apiculture, Agricultural University, 29 Listopada 54, 31-425 Krakow, Poland
*
*Author for correspondence Phone: +48 12 6625069 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite the fact that symmetry is common in nature, it is rarely perfect. Because there is a wide range of phenotypes which differs from the average one, the asymmetry should increase along with deviation. Therefore, the aim of this study was to assess the level of asymmetry in normal individuals as well as in phenodeviants categorized as minor or major based on abnormalities in forewing venation in honey bees. Shape fluctuating asymmetry (FA) was lower in normal individuals and minor phenodeviants compared with major phenodeviants, whereas the former two categories were comparable in drones. In workers and queens, there were not significant differences in FA shape between categories. FA size was significantly lower in normal individuals compared with major phenodeviant drones and higher compared with minor phenodeviant workers. In queens, there were no significant differences between categories. The correlation between FA shape and FA size was significantly positive in drones, and insignificant in workers and queens. Moreover, a considerable level of directional asymmetry was found as the right wing was constantly bigger than the left one. Surprisingly, normal individuals were significantly smaller than minor phenodeviants in queens and drones, and they were comparable with major phenodeviants in all castes. The correlation between wing size and wing asymmetry was negative, indicating that smaller individuals were more asymmetrical. The high proportion of phenodeviants in drones compared with workers and queens confirmed their large variability. Thus, the results of the present study showed that minor phenodeviants were not always intermediate as might have been expected.

Keywords

fluctuating asymmetrydirectional asymmetryphenodeviantshoney bees
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 3 , June 2016 , pp. 304 - 313
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abaga, N.O.Z., Alibert, P., Dousset, S., Savadogo, P.W., Savadogo, M. & Sedogo, M. (2011) Insecticide residues in cotton soils of Burkina Faso and effects of insecticides on fluctuating asymmetry in honey bees (Apis mellifera Linnaeus). Chemosphere 83(4), 585–592.CrossRefGoogle Scholar
Abou-Shaara, H.F. (2014) The foraging behaviour of honey bees, Apis mellifera: a review. Veterinarni Medicina 59(1), 1–10.Google Scholar
Akahira, Y. & Sakagami, S.F. (1959) Observations on the variability of wing venation in the honeybees. Journal of the Faculty of Science Hokkaido University Series VI Zoology 14(2), 175–184.Google Scholar
Babbitt, G.A., Kiltie, R. & Bolker, B. (2006) Are fluctuating asymmetry studies adequately sampled? Implications of a new model for size distribution. American Naturalist 167(2), 230–245.Google Scholar
Beasley, D.A.E., Bonisoli-Alquati, A. & Mousseau, T.A. (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecological Indicators 30, 218–226.Google Scholar
Bessoltane, N., Toffano-Nioche, C., Solignac, M. & Mougel, F. (2012) Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS ONE 7(5), e36229.CrossRefGoogle ScholarPubMed
Beye, M., Gattermeier, I., Hasselmann, M., Gempe, T., Schioett, M., Baines, J.F., Schlipalius, D., Mougel, F., Emore, C., Rueppell, O., Sirviö, A., Guzmán-Novoa, E., Hunt, G., Solignac, M. & Page, R.E. Jr. (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Research 16(11), 1339–1344.Google Scholar
Bienefeld, K., Reinhardt, F. & Pirchner, F. (1989) Inbreeding effects of queen and workers on colony traits in the honey bee. Apidologie 20(5), 439–450.CrossRefGoogle Scholar
Bitner-Mathé, B.C. & Klaczko, L.B. (1999) Heritability, phenotypic and genetic correlations of size and shape of Drosophila mediopunctata wings. Heredity 83(6), 688–696.Google Scholar
Bjorksten, T.A., Fowler, K. & Pomiankowski, A. (2000) What does sexual trait FA tell us about stress? Trends in Ecology and Evolution 15(4), 163–166.Google Scholar
Breuker, C.J., Patterson, J.S. & Klingenberg, C.P. (2006) A single basis for developmental buffering of Drosophila wing shape. PLoS ONE 1(1), e7.Google Scholar
Brückner, D. (1976) The influence of genetic variability on wing asymmetry in honey bees (Apis melliera). Evolution 30(1), 100–108.Google Scholar
Carter, A.J.R., Weier, T.M. & Houle, D. (2009) The effect of inbreeding on fluctuating asymmetry of wing veins in two laboratory strains of Drosophila melanogaster. Heredity 102(6), 563–572.Google Scholar
Casteel, D.B. & Phillips, E.F. (1903) Comparative variability of drones and workers of the honey bee. Biological Bulletin 6(1), 18–37.Google Scholar
Chapman, J.W. & Goulson, D. (2000) Environmental versus genetic influences on fluctuating asymmetry in the house fly, Musca domestica. Biological Journal of the Linnean Society 70(3), 403–413.Google Scholar
Clarke, G.M. (1997) The genetic basis of developmental stability. III. Haplodiploidy: are males more unstable than females? Evolution 51, 2021–2028.Google Scholar
Clarke, G.M. (1998 a) The genetic basis of developmental stability. IV. Individual and population asymmetry parameters. Heredity 80(5), 553–561.Google Scholar
Clarke, G.M. (1998 b) The genetic basis of developmental stability. V. Inter-and intra-individual character variation. Heredity 80(5), 562–567.Google Scholar
Clarke, G.M. & Oldroyd, B.P. (1996) The genetic basis of developmental stability in Apis mellifera II. Relationships between character size, asymmetry and single-locus heterozygosity. Genetica 97(2), 211–224.Google Scholar
Clarke, G.M., Brand, G.W. & Whitten, M.J. (1986) Fluctuating asymmetry: a technique for measuring developmental stress caused by inbreeding. Australian Journal of Biological Sciences 39(2), 145–154.Google Scholar
Clarke, G.M., Oldroyd, B.P. & Hunt, P. (1992) The genetic basis of developmental stability in Apis mellifera: heterozygosity versus genic balance. Evolution 46(3), 753–762.Google Scholar
Coelho, J.R. (1996) The flight characteristics of drones in relation to mating. BeeScience 4(1), 21–25.Google Scholar
Crespi, B.J. & Vanderkist, B.A. (1997) Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect. Heredity 79(6), 624–630.Google Scholar
De Block, M. & Stoks, R. (2007) Flight-related body morphology shapes mating success in a damselfly. Animal Behaviour 74(4), 1093–1098.Google Scholar
Fowler, K. & Whitlock, M.C. (1994) Fluctuating asymmetry does not increase with moderate inbreeding in Drosophila melanogaster. Heredity 73(4), 373–376.Google Scholar
Graham, J.H., Freeman, D.C. & Emlen, J.M. (1993) Developmental stability: a sensitive indicator of populations under stress. pp. 136–158in Landis, W.G., Hughes, J.S. & Lewis, M.A. (Eds) Environmental Toxicology and Risk Assessment. ASTM STP 1179. American Society for Testing and Materials, Philadelphia.Google Scholar
Graham, J.H., Fletcher, D., Tigue, J. & McDonald, M. (2000) Growth and developmental stability of Drosophila melanogaster in low frequency magnetic fields. Bioelectromagnetics 21(6), 465–472.Google Scholar
Graham, J.H., Raz, S., Hel-Or, H. & Nevo, E. (2010) Fluctuating asymmetry: methods, theory, and applications. Symmetry 2(2), 466–540.Google Scholar
Groenendijk, D., Zeinstra, L.W.M. & Postma, J.F. (1998) Fluctuating asymmetry and mentum gaps in populations of the midge Chironomus riparius (diptera: Chironomidae) from a metal-contaminated river. Environmental Toxicology and Chemistry 17(10), 1999–2005.Google Scholar
Heidinger, I.M.M., Meixner, M.D., Berg, S. & Büchler, R. (2014) Observation of the mating behavior of honey bee (Apis mellifera L.) queens using radio-frequency identification (RFID): factors influencing the duration and frequency of nuptial flights. Insects 5(3), 513–527.Google Scholar
Hrassnigg, N. & Crailsheim, K. (2005) Differences in drone and worker physiology in honeybees (Apis mellifera). Apidologie 36(2), 255–277.CrossRefGoogle Scholar
Imasheva, A.G., Bosenko, D.V. & Bubli, O.A. (1999) Variation in morphological traits of Drosophila melanogaster (fruit fly) under nutritional stress. Heredity 82(2), 187–192.Google Scholar
Jaffé, R. & Moritz, R.F.A. (2010) Mating flights select for symmetry in honeybee drones (Apis mellifera). Naturwissenschaften 97(3), 337–343.CrossRefGoogle ScholarPubMed
Jokela, P. & Portin, P. (1991) Effect of extra Y chromosome on number and fluctuating asymmetry of sternopleural bristles in Drosophila melanogaster. Hereditas 114(2), 177–187.Google Scholar
Jones, J.C., Helliwell, P., Beekman, M., Maleszka, R. & Oldroyd, B.P. (2005) The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera. Journal of Comparative Physiology A 191(12), 1121–1129.Google Scholar
Kamel, S.M., Osman, M.A.M., Mahmoud, M.F., Mohamed, K.M. & Abd Allah, S.M. (2013) Morphometric study of newly emerged unmated queens of honey bee Apis mellifera L. in Ismailia Governorate, Egypt. Arthropods 2(2), 80–88.Google Scholar
Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11(2), 353–357.Google Scholar
Klingenberg, C.P. & McIntyre, G.S. (1998) Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52(5), 1363–1375.Google Scholar
Klingenberg, C.P. & Monteiro, L.R. (2005) Distances and directions in multidimensional shape spaces: implications for morphometric applications. Systematic Biology 54(4), 678–688.Google Scholar
Koeniger, N. & Koeniger, G. (2007) Mating flight duration of Apis mellifera queens: as short as possible, as long as necessary. Apidologie 38(6), 606–611.CrossRefGoogle Scholar
Koeniger, N., Koeniger, G., Gries, M. & Tingek, S. (2005) Drone competition at drone congregation areas in four Apis species. Apidologie 36(2), 211–221.Google Scholar
Kruk, C. & Skowronek, W. (2002) Effect of different factors on the efficacy of honey bee queen rearing. Journal of Apicultural Science 46(1), 41–50.Google Scholar
Liu, H., Zhang, X., Huang, J., Chen, J.-Q., Tian, D., Hurst, L.D. & Yang, S. (2015) Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee. Genome Biology 16(1), 15.Google Scholar
Ludoški, J., Djurakic, M., Ståhls, G. & Milankov, V. (2012) Patterns of asymmetry in wing traits of three island and one continental population of Merodon albifrons (Diptera, Syrphidae) from Greece. Evolutionary Ecology Research 14(7), 933–950.Google Scholar
Ludoški, J., Djurakic, M., Pastor, B., Martinéz-Sánchez, A.I., Rojo, S. & Milankov, V. (2014) Phenotypic variation of the housefly, Musca domestica: amounts and patterns of wing shape asymmetry in wild populations and laboratory colonies. Bulletin of Entomological Research 104(1), 35–47.Google Scholar
Mahbobi, A., Farshineh-Adl, M., Woyke, J. & Abbasi, S. (2012) Effects of the age of grafted larvae and the effects of supplemental feeding on some morphological characteristics of Iranian queen honey bees (Apis mellifera meda Skorikov, 1929). Journal of Apicultural Science 56(1), 93–98.CrossRefGoogle Scholar
Markow, T.A. & Ricker, J.P. (1992) Male size, developmental stability, and mating success in natural populations of three Drosophila species. Heredity 69(2), 122–127.Google Scholar
Mather, K. (1953) Genetical control of stability in development. Heredity 7(3), 297–336.Google Scholar
Mazeed, A.M.M. (2011) Anomalies and asymmetry of wing venation pattern in Carniolan and Egyptian bee populations in Egypt. Egyptian Academic Journal of Biological Sciences 4(1), 149–161.Google Scholar
McLachlan, A. & Cant, M. (1995) Small males are more symmetrical: mating success in the midge Chironomus plumosus L. (Diptera: Chironomidae). Animal Behaviour 50(3), 841–846.Google Scholar
Messier, S. & Mitton, J.B. (1996) Heterozygosity at the malate dehydrogenase locus and developmental homeostasis in Apis mellifera. Heredity 76(6), 616–622.Google Scholar
Møller, A.P. & Swaddle, J.P. (1997) Asymmetry, Developmental Stability and Evolution. Oxford University Press Inc., New York.Google Scholar
Moritz, R.F.A. (1986) The origin of inbreeding depression in honeybees. Bee World 67(4), 157–163.Google Scholar
Owen, R.E. (1989) Differential size variation of male and female bumblebees. Journal of Heredity 80(1), 39–43.Google Scholar
Palmer, A.R. (1994) Fluctuating asymmetry analyses: a primer. pp. 335–364in Markow, T.A. (Ed.) Developmental Instability: Its Origins and Evolutionary Implications. Kluwer Academic Publishers, Dordrecht, Netherlands.Google Scholar
Palmer, A.R. & Strobeck, C. (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology and Systematics 17, 391–421.CrossRefGoogle Scholar
Palmer, A.R. & Strobeck, C. (2003) Fluctuating asymmetry analyses revisited. pp. 279–319in Polak, M., (Ed.) Developmental Instability (DI): Causes and Consequences. Oxford University Press, Oxford.Google Scholar
Pélabon, C. & Hansen, T.F. (2008) On the adaptive accuracy of directional asymmetry in insect wing size. Evolution 62(11), 2855–2867.Google Scholar
Polak, M. (1993) Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: implications for sexual selection. Genetica 89(1–3), 255–265.Google Scholar
Polak, M. & Taylor, P.W. (2007) A primary role of developmental instability in sexual selection. Proceedings of the Royal Society B: Biological Sciences 274(1629), 3133–3140.Google Scholar
Porporato, M., Laurino, D., Balzola, L. & Manino, A. (2014) Wing venation teratology in Apis mellifera L. Redia 97, 157–163.Google Scholar
Rasmuson, M. (1960) Frequency of morphological deviants as a criterion of developmental stability. Hereditas 46(3–4), 511–535.Google Scholar
Rohlf, F.J. & Slice, D. (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39(1), 40–59. DOI: 10.2307/2992207.Google Scholar
Ross, K.G. & Robertson, J.L. (1990) Developmental stability, heterozygosity, and fitness in two introduced fire ants (Solenopsis invicta and S. richteri) and their hybrid. Heredity 64(1), 93–103.Google Scholar
Ruttner, H. & Ruttner, F. (1972) Investigations of the flight activity and the mating behaviour of drones. V. – Drone congregation areas and mating distances. Apidologie 3(3), 203–232.Google Scholar
Schiff, N. & Sheppard, W. (1996) Genetic differentiation in the queen breeding population of the western United States. Apidologie 27(2), 77–86.Google Scholar
Schlüns, H., Moritz, R.F.A., Neumann, P., Kryger, P. & Koeniger, G. (2005) Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honeybee queens. Animal Behaviour 70(1), 125–131.Google Scholar
Schneider, S.S., Leamy, L.J., Lewis, L.A. & DeGrandi-Hoffman, G. (2003) The influence of hybridization between African and European honeybees, Apis mellifera, on asymmetries in wing size and shape. Evolution 57(10), 2350–2364.Google Scholar
Silva, M.C., Lomônaco, C., Augusto, S.C. & Kerr, W.E. (2009) Climatic and anthropic influence on size and fluctuating asymmetry of Euglossine bees (Hymenoptera, Apidae) in a semideciduous seasonal forest reserve. Genetics and Molecular Research 8(2), 730–737.Google Scholar
Smith, D.R., Crespi, B.J. & Bookstein, F.L. (1997) Fluctuating asymmetry in the honey bee, Apis mellifera: effects of ploidy and hybridization. Journal of Evolutionary Biology 10(4), 551–574.Google Scholar
Statsoft, Inc. (2011) Statistica (data analysis software system), version 10. www.statsoft.com.Google Scholar
Tan, K., Fuchs, S. & Engel, M.S. (2008) An adventitious distal abscissa in the forewing of honey bees (Hymenoptera: Apidae: Apis). Apidologie 39(6), 674–682.Google Scholar
Tofilski, A. (2014) DrawWing, Pro version 1.00. www.drawwing.orgGoogle Scholar
Tofilski, A. & Czekońska, K. (2014) Wing asymmetry of high and low quality honey bee queens. p. 15 in Proceedings of the COLOSS.2 Training School ‘‘Queen quality and breeding.’’ Thessaloniki, 2–4 March 2014.Google Scholar
Trotta, V., Calboli, F.C.F., Garoia, F., Grifoni, D. & Cavicchi, S. (2005) Fluctuating asymmetry as a measure of ecological stress in Drosophila melanogaster (Diptera: Drosophilidae). European Journal of Entomology 102(2), 195–200.Google Scholar
Vijendravarma, R.K., Narasimha, S. & Kawecki, T.J. (2011) Adaptation to larval malnutrition does not affect fluctuating asymmetry in Drosophila melanogaster. Biological Journal of the Linnean Society 104(1), 19–28.CrossRefGoogle Scholar
Węgrzynowicz, P., Gerula, D., Panasiuk, B. & Bieńkowska, M. (2009) Anomalies in wings of Apis Mellifera. Available online at http://www.inhort.pl/files/program_wieloletni/wykaz_publikacji/obszar6/Anomaliaskrzydel_Anomalies in wings of Apis mellifera.pdfGoogle Scholar
Zeldich, M., Swiderski, D. & Sheets, H. (2012) Geometric morphometrics for biologists: a primer. 2nd ed.n.Elsevier Academic Press, New York and London.Google Scholar
Zhou, B. & Zhu, X. (2009) The effect of temperature on hind wing vein of Apis cerana cerana during Sealed Brood's Development. Available online at http://www.apimondia.com/congresses/2009/Biology/Posters/The effect of temperature on hind wingvein-ZHOU Bingfeng.pdfGoogle Scholar