Gynandromorph of the squash bee Eucera (Peponapis) pruinosa (Hymenoptera: Apidae: Eucerini) from an agricultural field in western Pennsylvania, USA

Authors

  • Laura J Jones
  • Shelby Kerrin Kilpatrick
  • Margarita M López-Uribe

DOI:

https://doi.org/10.17161/jom.i100.13744

Abstract

Gynandromorphs are anomalous individuals that are genetically chimeric and express both male and female phenotypes. Here, we describe the first record of a mosaic gynandromorph of the squash bee Eucera (Peponapis) pruinosa (Say) from a single specimen collected from western Pennsylvania, United States of America (USA). We discuss the known developmental mechanisms resulting in gynandromorphism and how parasitism or environmental contaminants may instigate these mechanisms in wild bee individuals.

Metrics

Metrics Loading ...

References

Ayala, R., & T. Griswold. 2012. Two new species of the bee genus Peponapis, with a key to the North and Central American species (Hymenoptera: Apidae: Eucerini). Revista Mexicana de Biodiversidad 83(2): 396–406.

Beye, M., M. Hasselmann, M.K. Fondrk, R.E. Page, & S.W. Omholt. 2003. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114(4): 419–429.

Bossert, S., E.A. Murray, E.A. Almeida, S.G. Brady, B.B. Blaimer, & B.N. Danforth. 2019. Combining transcriptomes and ultraconserved elements to illuminate the phylogeny of Apidae. Molecular Phylogenetics and Evolution 130: 121–131.

Boveri, T. 1915. Über die Entstehung der Eugsterschen Zwitterbienen. Archiv für Entwicklungsmechanik der Organismen 41: 264–311.

Bridges, C.B., T.H. Morgan, & A.H. Sturtevant. 1919. Contributions to the Genetics of Drosophila melanogaster. Carnegie Institution of Washington; Washington, DC; v+388 pp., +12 pls.

Buczek, A., K. Bartosik, A.M. Buczek, W. Buczek, & D. Kulina. 2019. Abnormal development of Hyalomma marginatum ticks (Acari: Ixodidae) induced by plant cytotoxic substances. Toxins 11(8): 445.

Camargo, M.P., & R.B. Gonçalves. 2013. Register of a gynandromorph of Euglossa pleosticta Dressler (Hymenoptera, Apidae). Revista Brasileira de Entomologia 57(4): 424–426.

Chan, D.S.W., R.S. Prosser, J.L. Rodríguez-Gil, & N.E. Raine. 2019. Assessment of risk to hoary squash bees (Peponapis pruinosa) and other ground-nesting bees from systemic insecticides in agricultural soil. Scientific Reports 9(1): 1–13.

Chen, J., & C. Guô. 2008. Ecosystem Ecology Research Trends. Nova Science Publishers; New York, NY; xiii+364 pp.

Cockerell, T.D.A. 1906. Descriptions and records of bees.—X. Annals and Magazine of Natural History 17: 359–369.

Cothran, R.D., & M. Thiel, (Eds.). 2020. Natural History of the Crustacea [Volume 6]: Reproductive Biology: 394–428. Oxford University Press; Oxford, UK; 568 pp.

Dalla Torre, K.W., von, & H. Friese. 1899. Die hermaphroditen und gynandromorphen Hymenopteren. Berichte des Naturwissenschaftlich-medizinischen Vereins in Innsbruck 24: 1–96.

Dantchenko, A., T.C. Emmel, & A. Sourakov. 1995. Nuclear pollution and gynandromorphic butterflies in southern Russia. Holarctic Lepidoptera 2(2): 77–79.

Devillers, J. 2020. Fate and ecotoxicological effects of pyriproxyfen in aquatic ecosystems. Environmental Science and Pollution Research 27(14): 16052–16068.

Dorchin, A., M.M. López-Uribe, C.J. Praz, T. Griswold, & B.N. Danforth. 2018. Phylogeny, new generic-level classification, and historical biogeography of the Eucera complex (Hymenoptera: Apidae). Molecular Phylogenetics and Evolution 119: 81–92.

Dunn, A.M., T. Rigaud, & A.T. Ford. 2020. Environmental influences on Crustacean sex determination and reproduction: environmental sex determination, parasitism and pollution. In: Ford, A.T. 2012. Intersexuality in Crustacea: An environmental issue? Aquatic Toxicology 108: 125–129.

Giangarelli, D.C., G.A. Freiria, D.G. Ferreira, W.M. Aguiar, R.E.S. Penha, A.N. Alves, M.C. Gaglianone, & S.H. Sofia. 2015. Orchid bees: a new assessment on the rarity of diploid males in populations of this group of Neotropical pollinators. Apidologie 46(5): 606–617.

Gill, R.J., & N.E. Raine. 2014. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Functional Ecology 28(6): 1459–1471.

Gill, R.J., O. Ramos-Rodriguez, & N.E. Raine. 2012. Combined pesticide exposure severely affects individual-and colony-level traits in bees. Nature 491(7422): 105–108.

Grilo, T.F., & R. Rosa. 2017. Intersexuality in aquatic invertebrates: Prevalence and causes. Science of the Total Environment 592: 714–728.

Harpur, B.A., M. Sobhani, & A. Zayed. 2013. A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera. Entomologia Experimentalis et Applicata 146(1): 156–164.

Heimpel, G.E., & J.G. de Boer. 2008. Sex determination in the Hymenoptera. Annual Review of Entomology 53(1): 209–230.

Hinojosa-Díaz, I.A., V.H. Gonzalez, R. Ayala, J. Mérida, P. Sagot, & M.S. Engel. 2012. New orchid and leaf-cutter bee gynandromorphs, with an updated review (Hymenoptera, Apoidea). Zoosystematics and Evolution 88(2): 205–214.

Hiyama, A., C. Nohara, S. Kinjo, W. Taira, S. Gima, A. Tanahara, & J.M. Otaki. 2012. The biological impacts of the Fukushima nuclear accident on the pale grass blue butterfly. Scientific Reports 2(1): 1–11.

Huang, G.Y., W.J. Shi, G.Z. Fang, Y.-Q. Liang, Y.S. Liu, S.S. Liu, L.X. Hu, H.X. Chen, L. Xie, & G.G. Ying. 2020. Endocrine disruption in western mosquitofish from open and closed aquatic ecosystems polluted by swine farm wastewaters. Environment International 137: 105552.

Hurd, P.D., E.G. Linsley, & T.W. Whitaker. 1971. Squash and gourd bees (Peponapis, Xenoglossa) and the origin of the cultivated Cucurbita. Evolution 25(1): 218.

Kilpatrick, S.K., J. Gibbs, M.M. Mikulas, S-E. Spichiger, N. Ostiguy, D.J. Biddinger, & M.M. López-Uribe. 2020. An updated checklist of the bees (Hymenoptera, Apoidea, Anthophila) of Pennsylvania, United States of America. Journal of Hymenoptera Research 77: 1–86.

Krichilsky, E., Á. Vega-Hidalgo, K. Hunter, C. Kingwell, C. Ritner, W. Wcislo, & A. Smith. 2020. The first gynandromorph of the Neotropical bee Megalopta amoena (Spinola, 1853) (Halictidae) with notes on its circadian rhythm. Journal of Hymenoptera Research 75: 97–108.

Krupke, C.H., G.J. Hunt, B.D. Eitzer, G. Andino, & K. Given. 2012. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7(1): e29268.

LeBlanc, G.A. 2016. Overview of endocrine disruptor ecotoxicity in wildlife. In: Eldridge, J.C. & J.T. Stevens (Eds.), Endocrine Toxicology [3rd Edition]: 280–312. Informa Healthcare USA; New York, NY; 424 pp.

López-Uribe, M.M., M.T. Almanza, & M. Ordoñez. 2007. Diploid male frequencies in Colombian populations of euglossine bees. Biotropica 39(5): 660–662.

López-Uribe, M.M., J.H. Cane, R.L. Minckley, & B.N. Danforth. 2016. Crop domestication facilitated rapid geographical expansion of a specialist pollinator, the squash bee Peponapis pruinosa. Proceedings of the Royal Society B: Biological Sciences 283(1833): 20160443.

Lozier, J.D., & A. Zayed. 2017. Bee conservation in the age of genomics. Conservation Genetics 18(3): 713–729.

Lucia, M., & V.H. Gonzalez. 2013. A new gynandromorph of Xylocopa frontalis with a review of gynandromorphism in Xylocopa (Hymenoptera: Apidae: Xylocopini). Annals of the Entomological Society of America 106(6): 853–856.

Masuda, H. 1940. Biological notes on Eucera difficilis Pérez and whose [sic] parasitic bee, Nomada japonica Smith, with descriptions of a gynandromorphic Eucera. Kontyû 14: 45–60.

McGrady, C.M., R. Troyer, & S.J. Fleischer. 2020. Wild bee visitation rates exceed pollination thresholds in commercial Cucurbita agroecosystems. Journal of Economic Entomology 113(2): 562–574.

Michener, C.D. 2007. The Bees of the World [2nd Edition]. Johns Hopkins University Press; Baltimore, MD; xvi+[i]+953 pp., +20pls.

Michez, D., P. Rasmont, M. Terzo, & N.J. Vereecken. 2009. A synthesis of gynandromorphy among wild bees (Hymenoptera: Apoidea), with an annotated description of several new cases. Annales de la Société Entomologique de France 45(3): 365–375.

Morgan, T.H. 1916. The Eugster gynandromorph bees. American Naturalist 50(589): 39–45.

Narita, S., R.A.S. Pereira, F. Kjellberg, & D. Kageyama. 2010. Gynandromorphs and intersexes: potential to understand the mechanism of sex determination in arthropods. Terrestrial Arthropod Reviews 3(1): 63–96.

Olmstead, A.W., & G.A. LeBlanc. 2007. The environmental-endocrine basis of gynandromorphism (intersex) in a crustacean. International Journal of Biological Sciences 3(2): 77–84.

Ramos, K.S., & L. Ruz. 2013. First record of intersexual phenotype in Calliopsini bees (Hymenoptera, Apidae, Andreninae): An unusual specimen of Acamptopoeum submetallicum (Spinola). Zootaxa 3609(2): 239–242.

Salt, G. 1927. The effects of stylopization on aculeate Hymenoptera. Journal of Experimental Zoology 48(1): 223–331.

Schenau, E., & S. Jha. 2017. High levels of male diploidy but low levels of genetic structure characterize Bombus vosnesenskii populations across the western US. Conservation Genetics 18(3): 597–605.

Schneider, C.A., W.S. Rasband, & K.W. Eliceiri. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9(7): 671-675.

Scholz, S., & N. Klüver. 2009. Effects of endocrine disrupters on sexual, gonadal development in fish. Sexual Development 3(2–3): 136–151.

Shapiro, L.R., M. Youngblom, E.D. Scully, J. Rocha, J.N. Paulson, V. Klepac-Ceraj, A. Cibrián-Jaramillo, & M.M. López-Uribe. 2019. Bacterial communities of herbivores and pollinators that have co-evolved Cucurbita spp. BioRxiv 691378.

Spring, M.R., K.S. Lustofin, & M.M. Gardiner. 2015. Occurrence of a gynandromorphic Bombus bimaculatus (Hymenoptera: Apidae) in southeastern Ohio. Great Lakes Entomologist 48(3): 150–158.

Stern, C., & K. Sekiguti. 1931. Analyse eines Mosaikindividuums bei Drosophila melanogaster. Biologisches Zentralblatt 51: 194–199.

Stouthamer, R. 1997. Wolbachia-induced parthenogenesis. In: O’Neill, S.L., A.A. Hoffmann, & J.H. Werren (Eds.), Influential Passengers: Inherited Microorganisms and Arthropod Reproduction: 102–124. Oxford University Press; New York, NY; xi+214 pp.

Stouthamer, R., & D.J. Kazmer. 1994. Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73(3): 317–327.

Ullmann, K.S., M.H. Meisner, & N.M. Williams. 2016. Impact of tillage on the crop pollinating, ground-nesting bee, Peponapis pruinosa in California. Agriculture, Ecosystems and Environment 232: 240–246.

Urban, D. 1999. Ginandromorfia em Alloscirtetica brethesi (Joergensen) (Hymenoptera, Anthophoridae). Revista Brasileira de Zoologia 16: 171–173.

Van Wilgenburg, E., G. Driessen, & L.W. Beukeboom. 2006. Single locus complementary sex determination in Hymenoptera: An “unintelligent” design? Frontiers in Zoology 3: 1–15.

Villamizar, G. 2020. A new case of gynandromorphism in Xylocopa frontalis (Olivier) (Hymenoptera: Apidae), with an updated review of records in Xylocopinae Latreille. Revista Chilena de Entomología 46(2): 189–200.

Werren, J.H., L. Baldo, & M.E. Clark. 2008. Wolbachia: Master manipulators of invertebrate biology. Nature Reviews Microbiology 6(10): 741–751.

Zayed, A., & L. Packer. 2005. Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proceedings of the National Academy of Sciences, U.S.A. 102(30): 10742–10746.

Zayed, A., D.W. Roubik, & L. Packer. 2004. Use of diploid male frequency data as an indicator of pollinator decline. Proceedings of the Royal Society of London, Series B: Biological Sciences 271(Supplement 3): S9–S12.

Downloads

Published

24-02-2021

How to Cite

Jones, L., Kilpatrick, S., & López-Uribe, M. (2021). Gynandromorph of the squash bee Eucera (Peponapis) pruinosa (Hymenoptera: Apidae: Eucerini) from an agricultural field in western Pennsylvania, USA. Journal of Melittology, 100, 1-10. https://doi.org/10.17161/jom.i100.13744