Ploidy determination in Bombus terrestris males: cost-efficiency comparison among different techniques

References

• Ayabe, T., Hoshiba, H., & Ono, M. (2004). Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris. Chromosome Research : An International Journal on the Molecular, Supramolecular and Evolutionary Aspects of Chromosome Biology, 12(3), 215–223. https://doi.org/10.1023/b:chro.0000021880.83639.4b
   PubMed Web of Science ®Google Scholar
• Bogo, G., De Manincor, N., Fisogni, A., Galloni, M., & Bortolotti, L. (2017). Effects of queen mating status, pre-diapause weight and pupae’s sex on colony initiation in small-scale rearing of Bombus terrestris. Apidologie, 48(6), 845–854. https://doi.org/10.1007/s13592-017-0529-z
   Web of Science ®Google Scholar
• Bogo, G., De Manincor, N., Fisogni, A., Galloni, M., Zavatta, L., & Bortolotti, L. (2018). Different reproductive strategies and their possible relation to inbreeding risk in the bumble bee Bombus terrestris. Insectes Sociaux, 65(2), 289–295. https://doi.org/10.1007/s00040-018-0611-1
   Web of Science ®Google Scholar
• Bortolotti, L., Fiorillo, F., Zavatta, L., De Rogatis, A., & Bogo, G. (2020). Influence of inbreeding in the early stages of artificially reared colonies of Bombus terrestris. Journal of Applied Entomology, 144(7), 637–646.
   Web of Science ®Google Scholar
• Cejas, D., Ornosa, C., Muñoz, I., & De la Rúa, P. (2019). Preliminary report on cross-species microsatellite amplification for bumblebee biodiversity and conservation studies. Archivos de Zootecnia, 68, 428–432.
   Google Scholar
• Chapman, R. E., & Bourke, A. F. G. (2001). The influence of sociality on the conservation biology of social insects. Ecology Letters, 4(6), 650–662. https://doi.org/10.1046/j.1461-0248.2001.00253.x
   Web of Science ®Google Scholar
• Cook, J. M. (1993). Sex determination in the Hymenoptera: a review of models and evidence. Heredity, 71(4), 421–435. https://doi.org/10.1038/hdy.1993.157
   Web of Science ®Google Scholar
• Cook, J. M., & Crozier, R. H. (1995). Sex determination and population biology in the Hymenoptera. Trends in Ecology & Evolution, 10(7), 281–286. https://doi.org/10.1016/0169-5347(95)90011-x
   PubMed Web of Science ®Google Scholar
• Cowan, D. P., & Stahlhut, J. K. (2004 Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination. In Proceedings of the National Academy of Sciences (Vol. 101, pp. 10374–10379).
   Google Scholar
• Darvill, B., ÓConnor, S., Lye, G. C., Waters, J., Lepais, O., & Goulson, D. (2010). Cryptic differences in dispersal lead to differential sensitivity to habitat fragmentation in two bumblebee species. Molecular Ecology, 19(1), 53–63. https://doi.org/10.1111/j.1365-294X.2009.04423.x
   PubMed Web of Science ®Google Scholar
• De Boer, J. G., Ode, P. J., Vet, L. E. M., Whitfield, J. B., & Heimpel, G. E. (2007). Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis. Heredity, 99(3), 288–294. https://doi.org/10.1038/sj.hdy.6800995
   PubMed Web of Science ®Google Scholar
• Duchateau, M. J., Hoshiba, H., & Velthuis, H. H. W. (1994). Diploid males in the bumble-bee Bombus terrestris sex determination, sex alleles and viability. Entomologia Experimentalis et Applicata, 71(3), 263–269. https://doi.org/10.1111/j.1570-7458.1994.tb01793.x
   Web of Science ®Google Scholar
• Duchateau, M. J., & Mariën, J. (1995). Sexual biology of haploid and diploid males in the bumble bee Bombus terrestris. Insectes Sociaux, 42(3), 255–266. https://doi.org/10.1007/BF01240420
   Web of Science ®Google Scholar
• El Agoze, M., Drezen, J. M., Renault, S., & Periquet, G. (1994). Analysis of the reproductive potential of diploid males in the wasp Diadromus pulchellus (Hymenoptera, Ichneumonidae). Bulletin of Entomological Research, 84(2), 213–218. https://doi.org/10.1017/S0007485300039717
   Web of Science ®Google Scholar
• Ellis, J. S., Knight, M. E., Darvill, B., & Goulson, D. (2006). Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Molecular Ecology, 15(14), 4375–4386. https://doi.org/10.1111/j.1365-294X.2006.03121.x
   PubMed Web of Science ®Google Scholar
• Estoup, A., Scholl, A., Pouvreau, A., & Solignac, M. (1995). Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Molecular Ecology, 4(1), 89–93. https://doi.org/10.1111/j.1365-294x.1995.tb00195.x
   PubMed Web of Science ®Google Scholar
• Estoup, A., Solignac, M., Cornuet, J.-M., Goudet, J., & Scholl, A. (1996). Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Molecular Ecology, 5(1), 19–31. https://doi.org/10.1111/j.1365-294X.1996.tb00288.x
   PubMed Web of Science ®Google Scholar
• Estoup, A., Solignac, M., Harry, M., & Cornuet, J. M. (1993). Characterization of (GT)n and (CT)n microsatellites in two insect species: Apis mellifera and Bombus terrestris. Nucleic Acids Research, 21(6), 1427–1431. https://doi.org/10.1093/nar/21.6.1427
   PubMed Web of Science ®Google Scholar
• Gerard, M., Michez, D., Fournier, D., Maebe, K., Smagghe, G., Biesmeijer, J. C., & De Meulemeester, T. (2015). Discrimination of haploid and diploid males of Bombus terrestris (Hymenoptera; Apidae) based on wing shape. Apidologie, 46(5), 644–653. https://doi.org/10.1007/s13592-015-0352-3
   Web of Science ®Google Scholar
• Gerloff, C. U., Ottmer, B. K., & Schmid-Hempel, P. (2003). Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Functional Ecology, 17(5), 582–589. https://doi.org/10.1046/j.1365-2435.2003.00769.x
   Web of Science ®Google Scholar
• Gerloff, C. U., & Schmid-Hempel, P. (2005). Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos, 111(1), 67–80. https://doi.org/10.1111/j.0030-1299.2005.13980.x
   Web of Science ®Google Scholar
• Gosterit, A. (2016). Adverse effect of inbreeding on colony foundation success in bumblebee, Bombus terrestris (Hymenoptera: Apidae). Applied Entomology and Zoology, 51(4), 521–526. https://doi.org/10.1007/s13355-016-0427-2
   Web of Science ®Google Scholar
• Heimpel, G. E., & De Boer, J. G. (2008). Sex determination in the Hymenoptera. Annual Review of Entomology, 53, 209–230. https://doi.org/10.1146/annurev.ento.53.103106.093441
   PubMed Web of Science ®Google Scholar
• Hermann, M., Trenzcek, T., Fahrenhorst, H., & Engels, W. (2005). Characters that differ between diploid and haploid honey bee (Apis mellifera) drones. Genetics and Molecular Research, 4, 624–641.
   PubMedGoogle Scholar
• Hingston, A. B. (2005). Inbreeding in the introduced bumblebee Bombus terrestris causes uncertainty in predictions of impacts on native ecosystems. Ecological Management & Restoration, 6, 151–153.
   Google Scholar
• Hoshiba, H., Duchateau, M. J., & Velthuis, H. H. W. (1995). Diploid males in the bumble bee Bombus terrestris (Hymenoptera) karyotype analyses of diploid females, diploid males and haploid males. Japanese Journal of Entomology, 63, 203–207.
   Google Scholar
• Klingenberg, C. P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
   PubMed Web of Science ®Google Scholar
• Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution; International Journal of Organic Evolution, 52(5), 1363–1375. https://doi.org/10.1111/j.1558-5646.1998.tb02018.x
   PubMed Web of Science ®Google Scholar
• Kozmus, P., Virant-Doberlet, M., Meglič, V., & Dovč, P. (2011). Identification of Bombus species based on wing venation structure. Apidologie, 42(4), 472–480. https://doi.org/10.1007/s13592-011-0037-5
   Web of Science ®Google Scholar
• Krieger, M. J. B., Ross, K. G., Chang, C. W. Y., & Keller, L. (1999). Frequency and origin of triploidy in the fire ant Solenopsis invicta. Heredity, 82(2), 142–150. https://doi.org/10.1038/sj.hdy.6884600
   Web of Science ®Google Scholar
• Kukuk, P. F., & May, B. (1990). Diploid males in a primitively eusocial bee, Lasioglossum (Dialictus) zephyrum. Evolution, 44, 1522–1528.
   PubMed Web of Science ®Google Scholar
• Lecocq, T., Gérard, M., Maebe, K., Brasero, N., Dehon, L., Smagghe, G., Valterová, I., De Meulemeester, T., Rasmont, P., & Michez, D. (2017). Chemical reproductive traits of diploid Bombus terrestris males: Consequences on bumblebee conservation. Insect Science, 24(4), 623–630. https://doi.org/10.1111/1744-7917.12332
   PubMed Web of Science ®Google Scholar
• Liebert, A. E., Sumana, A., & Starks, P. T. (2005). Diploid males and their triploid offspring in the paper wasp Polistes dominulus. Biology Letters, 1(2), 200–203. https://doi.org/10.1098/rsbl.2004.0284
   PubMed Web of Science ®Google Scholar
• Lodesani, M., Balduzzi, D., & Galli, A. (2004). Functional characterisation of semen in honeybee queen (A. m. ligustica S.) spermatheca and efficiency of the diluted semen technique in instrumental insemination. Italian Journal of Animal Science, 3(4), 385–392. https://doi.org/10.4081/ijas.2004.385
   Google Scholar
• Maebe, K., Karise, R., Meeus, I., Mänd, M., & Smagghe, G. (2019). Pattern of population structuring between Belgian and Estonian bumblebees. Scientific Reports, 9(1), 9651. https://doi.org/10.1038/s41598-019-46188-7
   PubMed Web of Science ®Google Scholar
• Maebe, K., Meeus, I., Ganne, M., Wäckers, F., & Smagghe, G. (2014). Scientific note on microsatellite DNA analyses revealing diploid and haploid drones in bumblebee mass breeding. Apidologie, 45(2), 189–191. https://doi.org/10.1007/s13592-013-0237-2
   Web of Science ®Google Scholar
• Maebe, K., Meeus, I., Maharramov, J., Grootaert, P., Michez, D., Rasmont, P., & Smagghe, G. (2013). Microsatellite analysis in museum samples reveals inbreeding before the regression of Bombus veteranus. Apidologie, 44(2), 188–197. https://doi.org/10.1007/s13592-012-0170-9
   Web of Science ®Google Scholar
• Martínez, A. S., Rousselot, N., Corley, J. C., & Masciocchi, M. (2021). Nest-departure behaviour of gynes and drones in the invasive yellowjacket Vespula germanica (Hymenoptera: Vespidae). Bulletin of Entomological Research, 111(2), 174–181.
   Google Scholar
• Müller, C., & Schmid-Hempel, P. (1992). Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites. Ecological Entomology, 17(4), 343–353. https://doi.org/10.1111/j.1365-2311.1992.tb01068.x
   Web of Science ®Google Scholar
• Naito, T., & Suzuki, H. (1991). Sex determination in the sawfly, Athalia rosae ruficornis (Hymenoptera): occurrence of triploid males. Journal of Heredity, 82(2), 101–104. https://doi.org/10.1093/oxfordjournals.jhered.a111042
   Web of Science ®Google Scholar
• Owen, R. (1988). Body size variation and optimal body size of bumble bee queens (Hymenoptera: Apidae). The Canadian Entomologist, 120(1), 19–27. https://doi.org/10.4039/Ent12019-1
   Web of Science ®Google Scholar
• Paxton, R. J., Bego, L. R., Shah, M. M., & Mateus, S. (2003). Low mating frequency of queens in the stingless bee Scaptotrigona postica and worker maternity of males. Behavioral Ecology and Sociobiology, 53(3), 174–181. https://doi.org/10.1007/s00265-002-0561-4
   Web of Science ®Google Scholar
• Plowright, R. C., & Pallett, M. J. (1979). Worker-male conflict and inbreeding in bumble bees (Hymenoptera: Apidae). The Canadian Entomologist, 111(3), 289–294. https://doi.org/10.4039/Ent111289-3
   Web of Science ®Google Scholar
• Potts, S., Imperatriz-Fonseca, V., Ngo, H. T., Aizen, M. A., Biesmeijer, J. C., Breeze, T. D., Dicks, L. V., Garibaldi, L. A., Hill, R., Settele, J., & Vanbergen, A. J. (2016). Safeguarding pollinators and their values to human well-being. Nature, 540(7632), 220–229. https://doi.org/10.1038/nature20588
   PubMed Web of Science ®Google Scholar
• Queller, D. C., Strassmann, J. E., & Hughes, C. R. (1993). Microsatellites and kinship. Trends in Ecology & Evolution, 8(8), 285–288. https://doi.org/10.1016/0169-5347(93)90256-O
   PubMed Web of Science ®Google Scholar
• Reber Funk, C., Schmid-Hempel, R., & Schmid-Hempel, P. (2006). Microsatellite loci for Bombus spp. Molecular Ecology Notes, 6(1), 83–86. https://doi.org/10.1111/j.1471-8286.2005.01147.x
   Web of Science ®Google Scholar
• Rohlf, F. J. (2015). The tps series of software. HYSTRIX, 26, 9–12.
   Web of Science ®Google Scholar
• Santomauro, G., Oldham, N. J., Boland, W., & Engels, W. (2004). Cannibalism of diploid drone larvae in the honey bee (Apis mellifera) is released by odd pattern of cuticular substances. Journal of Apicultural Research, 43(2), 69–74. https://doi.org/10.1080/00218839.2004.11101114
   Web of Science ®Google Scholar
• Schlüns, H., Schlüns, E. A., van Praagh, J., & Moritz, R. F. A. (2003). Sperm numbers in drone honeybees (Apis mellifera) depend on body size. Apidologie, 34(6), 577–584. https://doi.org/10.1051/apido:2003051
   Web of Science ®Google Scholar
• Schmid-Hempel, R., & Schmid-Hempel, P. (2000). Female mating frequencies in Bombus spp. from Central Europe. Insectes Sociaux, 47(1), 36–41. https://doi.org/10.1007/s000400050006
   Web of Science ®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. https://doi.org/10.1007/s000360050041
   Web of Science ®Google Scholar
• Takahashi, J., Ayabe, T., Mitsuhata, M., Shimizu, I., & Ono, M. (2008). Diploid male production in a rare and locally distributed bumblebee, Bombus florilegus (Hymenoptera, Apidae). Insectes Sociaux, 55(1), 43–50. https://doi.org/10.1007/s00040-007-0976-z
   Web of Science ®Google Scholar
• Tasei, J. N., Moinard, C., Moreau, L., Himpens, B., & Guyonnaud, S. (1998). Relationship between aging, mating and sperm production in captive Bombus terrestris. Journal of Apicultural Research, 37(2), 107–113. https://doi.org/10.1080/00218839.1998.11100962
   Web of Science ®Google Scholar
• van Wilgenburg, E., Driessen, G., & Beukeboom, L. W. (2006). Single locus complementary sex determination in Hymenoptera: an "unintelligent" design? Frontiers in Zoology, 3(1), 1. https://doi.org/10.1186/1742-9994-3-1
   PubMedGoogle Scholar
• Velthuis, H. H. W., & Van Doorn, A. (2006). A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37(4), 421–451. https://doi.org/10.1051/apido:2006019
   Web of Science ®Google Scholar
• Whitehorn, P. R., Tinsley, M. C., Brown, M. J. F., Darvill, B., & Goulson, D. (2009). Impacts of inbreeding on bumblebee colony fitness under field conditions. BMC Evolutionary Biology, 9, 152. https://doi.org/10.1186/1471-2148-9-152
   PubMed Web of Science ®Google Scholar
• Woyke, J. (1963). What happens to the diploid drone larvae in a honeybee colony. Journal of Apicultural Research, 2(2), 73–75. https://doi.org/10.1080/00218839.1963.11100063
   Google Scholar
• Zayed, A., & Packer, L. (2001). High levels of diploid male production in a primitively eusocial bee (Hymenoptera: Halictidae). Heredity, 87(Pt 6), 631–636. https://doi.org/10.1046/j.1365-2540.2001.00952.x
   PubMed Web of Science ®Google Scholar
• Zayed, A., & Packer, L. (2005 Complementary sex determination substantially increases extinction proneness of haplodiploid populations. In Proceedings of the National Academy of Sciences (Vol. 102, pp. 10742–10746).
   Google Scholar
• Zayed, A., Roubik, D. W., & Packer, L. (2004 Use of diploid male frequency data as an indicator of pollinator decline [Paper presentation]. In Proceedings of the Royal Society B (Vol. 271, pp. 9–12).
   Google Scholar