Abstract
A commercialized pollinator introduced from Europe, Bombus terrestris, has colonized Japan. We investigated nest density and genetic structure in two sites based on worker genotypes at 12 microsatellite loci. We confirmed that five workers were triploids using multilocus genotypes and flow cytometry, indicating that queens mated with diploid males and produced triploid workers. The inbreeding coefficient of diploid workers representing individual colonies was significantly positive (F IS = 0.048) in a site where triploids were found. Genetic diversity in the sites was as high as that in native regions in Europe, and genetic differentiation between the sites was low (F ST = 0.006). The maximum distance between sampling locations of full-sib worker pairs indicated that the radius of a foraging range was at least 782 m. The estimates of nest density were 31 and 89 km−2 in the two sites, suggesting that the nest density in a colonized region can be higher than that in the native regions.
Zusammenfassung
Die kommerziell aus Europa eingeführte Bestäuberart Bombus terrestris hat sich inzwischen über ganz Japan verbreitet und beeinflusst dadurch möglicherweise einheimische Bienenund Pflanzenarten. In den Verbreitungsgebieten scheint die genetische Diversität geringer zu sein als in ursprünglichen Regionen, da die Gründerpopulationen meist recht klein sind. Durch Inzucht in kleinen Gründerpopulationen entstehen diploide Männchen, die bei der Paarung triploide Individuen zeugen. Trotz der Inzucht und der verringerten genetischen Variabilität vergrößern wilde Populationen ihr Verbreitungsgebiet und kommen dann teilweise recht häufig vor. Wir untersuchten die Nestdichte und die genetische Struktur bestimmter Genotypen an zwei Untersuchungsstandorten in Nordjapan auf der Basis von 12 Mikrosatelliten-Loci von sammelnden Arbeiterinnen (Abb. 1). Wir bestätigten anhand von Multilocus-Genotypanalysen, dass fünf Arbeiterinnen triploid waren (Abb. 2); deren Königinnen hatten sich vermutlich mit diploiden Männchen verpaart und danach triploide Arbeiterinnen produziert. Die Ergebnisse lassen Inzucht vermuten. Folgerichtig war der Inzuchtkoeffizient von diploiden Arbeiterinnen aus Einzelvölkern signifikant positiv (F IS = 0, 048), wenn an den Standorten triploide Arbeiterinnen gefunden wurden (Tab. II). Die genetische Diversität an diesen Standorten war genauso hoch wie in den Ursprungsregionen in Europa und die genetische Differenzierung zwischen den Standorten war gering (F ST = 0, 006; Tab. II). Diese Ergebnisse lassen vermuten, dass diese Wildpopulationen von verschiedenen Linien kommerziell eingeführter Völker abstammen und dass es durch Migration zur Vermischung verschiedener Populationen kam. Die maximale Distanz zwischen Sammelorten von Vollgeschwister-Paaren zeigt, dass der Sammelradius mindestens 782 m beträgt (Abb. 3). Die geschätzte Nestdichte von 31 und 89 km−2 an zwei verschiedenen Standorten (Tab. I) zeigt, dass die Dichte im neuen Verbreitungsgebiet höher sein kann als in den Ursprungsregionen. Unsere Befunde lassen vermuten, dass reduzierte Paarungsmöglichkeiten für die Inzucht in eingeschleppten B. terrestris-Populationen verantwortlich sind.
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References
Aron S., de Menten L., Van Bockstaele D.R., Blank S.M., Roisin Y. (2005) When hymenopteran males reinvented diploidy, Curr. Biol. 15, 824–827.
Ayabe T., Hoshiba H., Ono M. (2004) Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris, Chromosome Res. 12, 215–223.
Buttermore R.E., Pomeroy N., Hobson W., Semmens T., Hart R. (1998) Assessment of the genetic base of Tasmanian bumble bees (Bombus terrestris) for development as pollination agents., J. Apic. Res. 37, 23–25.
Chapman R.E., Bourke A.F.G. (2001) The influence of sociality on the conservation biology of social insects, Ecol. Lett. 4, 650–662.
Chapman R.E., Wang J., Bourke A.F.G. (2003) Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators, Mol. Ecol. 12, 2801–2808.
Cresswell J.E., Osborne J.L., Goulson D. (2000) An economic model of the limits to foraging range in central place foragers with numerical solutions for bumblebees, Ecol. Entomol. 25, 249–255.
Darvill B., Knight M.E., Goulson D. (2004) Use of genetic markers to quantify bumblebee foraging range and nest density, Oikos 107, 471–478.
Darvill B., Ellis J.S., Lye G.C., Goulson D. (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae), Mol. Ecol. 15, 601–611.
Duchateau M.J., Marien J. (1995) Sexual biology of haploid and diploid males in the bumble bee Bombus terrestris, Insectes Soc. 42, 255–266.
Duchateau M.J., Hoshiba H., Velthuis H.H.W. (1994) Diploid males in the bumble bee Bombus terrestris: Sex determination, sex alleles and viability, Entomol. Exp. Appl. 71, 263–269.
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), Mol. Ecol. 15, 4375–4386.
Estoup A., Scholl A., Pouvreau A., Solignac M. (1995) Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites, Mol. Ecol. 4, 89–93.
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, Mol. Ecol. 5, 19–31.
Funk C.R., Schmid-Hempel R., Schmid-Hempel P. (2006) Microsatellite loci for Bombus spp., Mol. Ecol. Notes 6, 83–86.
Goka K., Okabe K., Yoneda M. (2006) Worldwide migration of parasitic mites as a result of bumblebee commercialization, Popul. Ecol. 48, 285–291.
Goudet J. (2002) FSTAT: A program to estimate and test gene diversities and fixation indices (version 2.9) [online] http://www2.unil.ch/popgen/softwares/fstat.htm (accessed on 12 January 2009).
Goulson D. (2003) Effects of introduced bees on native ecosystems, Annu. Rev. Ecol. Evol. Syst. 34, 1–26.
Goulson D., Stout J.C. (2001) Homing ability of the bumblebee Bombus terrestris (Hymenoptera: Apidae), Apidologie 32, 105–111.
Hingston A.B. (2005) Inbreeding in the introduced Bumblebee Bombus terrestris causes uncertainty in predictions of impacts on native ecosystems, Ecol. Manage. Restor. 6, 149–153.
Hingston A.B. (2006) Is the exotic bumblebee Bombus terrestris really invading Tasmanian native vegetation? J. Insect Conserv. 10, 289–293.
Hingston A.B., Herrmann W., Jordan G.J. (2006) Reproductive success of a colony of the introduced bumblebee Bombus terrestris (L.) (Hymenoptera: Apidae) in a Tasmanian National Park, Aust. J. Entomol. 45, 137–141.
Hoffman J.I., Amos W. (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion, Mol. Ecol. 14, 599–612.
Inari N., Nagamitsu T., Kenta T., Goka K., Hiura T. (2005) Spatial and temporal pattern of introduced Bombus terrestris abundance in Hokkaido, Japan, and its potential impact on native bumblebees, Popul. Ecol. 47, 77–82.
Inoue M.N., Yokoyama J., Washitani I. (2007) Displacement of Japanese native bumblebees by the recently introduced Bombus terrestris (L.) (Hymenoptera: Apidae), J. Insect Conserv. 12, 135–146
Keane R.M., Crawley M.J. (2002) Exotic plant invasions and the enemy release hypothesis, Trends Ecol. Evol. 17, 164–170.
Kenta T., Inari N., Nagamitsu T., Goka K., Hiura T. (2007) Commercialized European bumblebee can cause pollination disturbance: an experiment on seven native plant species in Japan, Biol. Conserv. 134, 298–309.
Knight M.E., Martin A.P., Bishop S., Osborne J.L., Hale R.J., Sanderson R.A., Goulson D. (2005) An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species, Mol. Ecol. 14, 1811–1820.
Kunitake Y., Goka K. (2006) Environmental risk assessment and management decisions for introduced insects: Legal controls on Bombus terrestris by Invasive Alien Species Act, Jap. J. Plant Prot. 60, 196–197.
Matsumura C., Yokoyama J., Washitani I. (2004) Invasion status and potential ecological impacts of an invasive alien bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) naturalized in southern Hokkaido, Japan, Global Environ Res. 8, 51–66.
Nagamitsu T., Kenta T., Inari N., Goka K., Hiura T. (2007a) Foraging interactions between native and exotic bumblebees: Enclosure experiments using native flowering plants, J. Insect Conserv. 11, 123–130.
Nagamitsu T., Kenta T., Inari N., Kato E., Hiura T. (2007b) Abundance, body size, and morphology of bumblebees in an area where an exotic species, Bombus terrestris, has colonized in Japan, Ecol. Res. 22, 331–341.
Nakajima M., Matsumura C., Yokoyama J., Washitani I. (2004) Nesting in Bombus terrestris (Linnaeus) and foraging by B. terrestris workers from a B. hypocrita sapporoensis (Cockerell) nest in Mukawa-cho, Yufutsu-gun, Hokkaido, Japan, Jap. J. Conserv. Ecol. 9, 57–63.
Nei M. (1987) Molecular Evolutionary Genetics, Columbia University Press, New York.
Oldroyd B.P., Thexton E.G., Lawler S.H., Estoup A., Crozier R. (1995) Population demography of Australian feral bees (Apis mellifera), Oecologia 111, 381–387.
Osborne J.L., Clark S.J., Morris R.J., Williams I.H., Riley J.R., Smith A.D., Reynolds D.R., Edwards A.S. (1999) A Landscape-scale study of bumble bee foraging range and constancy, using harmonic radar, J. Appl. Ecol. 36, 519–533.
Piry S., Luikart G., Cornuet J.-M. (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data., J. Hered. 90, 502–503.
R Development Core Team (2006) R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, [online] http://www.R-project.org/foundation (accessed on 12 January 2009).
Roubik D.W. (1983) Experimental community studies: time-series tests of competition between African and Neotropical bees, Ecology 64, 971–978.
Schmid-Hempel P., Schmid-Hempel R., Brunner P., Seeman O., Allen G. (2007) Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck, Heredity 99, 414–422.
Schmid-Hempel R., Schmid-Hempel P. (2000) Female mating frequencies in Bombus spp. from central Europe, Insectes Soc. 47, 36–41.
Walsh P., Metzger D., Higuchi R. (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material, Biotechniques 10, 506–513.
Walther-Hellwig K., Frankl R. (2000) Foraging habitats and foraging distances of bumblebees, Bombus spp. (Hym., Apidae), in an agricultural landscape, J. Appl. Entomol. 124, 299–306.
Wang J. (2004) Sibship reconstruction from genetic data with typing errors, Genetics 166, 1963–1979.
Widmer A., Schmid-Hempel P. (1999) The population genetic structure of a large temperate pollinator species, Bombus pascuorum (Scopoli) (Hymenoptera: Apidae), Mol. Ecol. 8, 387–398.
Widmer A., Schmid-Hempel P., Estoup A., Scholl A. (1998) Population genetic structure and colonization history of Bombus terrestris s.l. (Hymenoptera: Apidae) from the Canary Islands and Madeira, Heredity 81, 563–572.
Weir B.S., Cockerham C.C. (1984) Estimating F-statistics for the analysis of population structure, Evolution 38, 1358–1370.
Wright S. (1951) The genetical structure of populations, Ann. Eugen. 15, 323–354.
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Nagamitsu, T., Yamagishi, H. Nest density, genetic structure, and triploid workers in exotic Bombus terrestris populations colonized Japan. Apidologie 40, 429–440 (2009). https://doi.org/10.1051/apido/2009004
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DOI: https://doi.org/10.1051/apido/2009004