Abstract
Loss of habitat and chemical use associated with agriculture can cause population declines of wild pollinators. Less is known about the evolutionary consequences of interactions between species used in commercial agriculture and wild pollinators. Given population declines of many wild bee species, it is crucial to understand if commercial queens become established in natural areas, if wild bees visit agricultural fields and have the potential to interact with commercial bees, and if gene flow occurs between commercial and wild bees. We drew on a long-term data set that documents commercial bumble bee (Bombus impatiens) use in New England, and we conducted genetic analyses of foraging B. impatiens from areas with varying intensities of commercial bee use. In agricultural areas with a history of commercial bee use we also sampled bees directly from commercial hives. We found significant genetic differences among foraging B. impatiens and B. impatiens sampled directly from hives (average pairwise F′ST = 0.14), but not among samples of foraging bees from natural areas (average F′ST among foraging bees = 0.002). Furthermore, Bayesian analysis of population structure revealed that foraging bees caught in areas with a history of commercial bee use grouped with samples from natural areas. These results document an agricultural setting where there was no widespread introgression of alleles from commercial bumble bees to wild bumble bees, commercial bumble bees did not become established in natural areas, and wild bees were providing pollination services to crops.
Similar content being viewed by others
References
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Benjamin FE, Winfree R (2014) Lack of pollinators limits fruit production in commercial blueberry (Vaccinium corymbosum). Environ Entomol 43:1574–1583
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 4:1165–1188
Biesmeijer JC, Roberts SPM, Reemer M, Ohlemueller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354
Blacher P, Yagound B, Lecoutey E, Devienne P, Chameron S, Chaline N (2013) Drifting behavior as an alternative reproductive strategy for social insect workers. Proc R Soc Lond. doi:10.1098/rspb.2013.1888
Byatt MA, Chapman NC, Latty T, Oldroyd BP (2016) The genetic consequences of the anthropogenic movement of social bees. Insect Soc 63:15–24
Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. Proc Nat Acad Sci USA 108:662–667
Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461–467
Dafni A, Kevan P, Gross CL, Goka K (2010) Bombus terrestris, pollinator, invasive and pest: an assessment of problems associated with its widespread introductions for commercial purposes. App Entomol Zool 45:101–113
Darvill B, O’Connor S, Lye GC, Waters J, Lepais O, Goulson D (2010) Cryptic differences in dispersal lead to differential sensitivity to habitat fragmentation in two bumblebee species. Mol Ecol 19:53–63
Delaplane KS, Mayer DF (2000) Crop pollination by Bees Wallingford. CABI, UK
Desneux N, Decourtye A, Delpuech J-M (2007) The effects of sub lethal doses of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Dreier S, Redhead JW, Warren IA, Bourke AFG, Heard MS, Jordan WC, Sumner S, Wang J, Carvell C (2014) Fine-scale spatial genetic structure of common and declining bumble bee species across an agricultural landscape. Mol Ecol 23:3384–3395
Earl DA, vonHoldt BM (2011) Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Con Gen Res 4:259–361
Edmans S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475
Estoup A, Scholl A, Pouvreau A, Solignac M (1995) Monandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol Ecol 4:89–93
Estoup A, Solignac M, Cornuet JM, Goudet J, Scholl A (1996) Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol Ecol 5:19–31
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
FAO 2015. Available at: http://faostat3.fao.org/home/E
Frankham R, Ballou JD, Eldridge MD, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475
Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366
Geiger F, Bengtsson J, Berendse F, Weisser WW, Emmerson M, Morales MB (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic App Ecol 11:97–105
Genersch E, Yue C, Fries I, de Miranda JR (2006) Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J Invert Pathol 91:61–63
Glantz SA, Slinker BY (2001) Applied regression and analysis of variance. McGraw-Hill, New York
Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186
Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Ann Rev Entomol 53:191–208
Goulson D, Kaden JC, Lepais O, Lye GC, Darvill B (2011) Population structure, dispersal and colonization history of the garden bumblebee Bombus hortorum in the western Isles of Scotland. Con Gen 12:867–879
Green RE, Cornell SJ, Scharlemann JPW, Balmford A (2005) Farming and the fate of wild nature. Science 307:550–555
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol. Ecol Res 9:1322–1332
Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155
Jha S (2015) Contemporary human-altered landscapes and oceanic barriers reduce bumble bee gene flow. Mol Ecol 24:993–1006
Jha S, Kremen C (2013a) Bumble bee foraging in response to landscape heterogeneity. Proc Natl Acad Sci 110:555–558
Jha S, Kremen C (2013b) Urban land use limits regional bumble bee gene flow. Mol Ecol 22:2483–2495
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026
Kanbe Y, Okada I, Yoneda M, Goka K, Tsuchida K (2008) Interspecific mating of the introduced bumblebee Bombus terrestris and the native Japanese bumblebee Bombus hypocrita sapporoensis results in inviable hybrids. Naturwissenschaften 95:1003–1008
Kevan PG, Phillips TP (2001) The economic impacts of pollinator declines: an approach to assessing the consequences. Conserv Ecol 5:8
Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Ser B 274:1608
Koh LP, Wilcove DS (2008) Is oil palm agriculture really destroying tropical biodiversity? Conserv Lett 1:60–64
Kraus FB, Szentgyörgyi H, Rożej E, Rhode M, Moroń D, Woyciechowski M, Moritz RFA. (2011) Greenhouse bumble bees (Bombus terrestris) spread their genes into the wild. Con Gen 12:187–192
Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci USA 99:16812–16816
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201
Lepais O, Darvill B, O’Connor S, Osborne JL, Sanderson RA, Cussans J, Goffe L, Goulson D (2010) Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol Ecol 19:819–831
Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. BioSience 56:311–323
Lozier JD, Strange JP, Stewart IJ, Cameron SA (2011) Patterns of range-wide genetic variation in six north american bumble bee (Apidae: Bombus) species. Mol Ecol 20:4870–4888
Manley R, Boots M, Wilfert L (2015) Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors. J App Ecol 52:331–340
Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Mol. Ecol Res 11:5–18
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Narum SR (2006) Beyond Bonferroni: less conservative analyses for landscape genetics. Con Gen 7:783–787
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Ollerton J, Tarrant S, Winfree R (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326
Paini DR, Williams MR, Roberts JD (2005) No short-term impact of honey bees on the reproductive success of an Australian native bee. Apidologie 36:613–621
Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts, and drivers. Trends Ecol Evol 25:345–353
Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Reber Funk C, Schmid-Hempel R, Schmid-Hempel P (2006) Microsatellite loci for Bombus sp. Mol Ecol Notes 6:83–86
Ricketts TH et al (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515
Rodriguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol. Ecol Res 12:873–884
Röseler PF (1985) A technique for year-round rearing of Bombus terrestris (Apidae, Bombini) colonies in captivity. Apidologie 16:165–170
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol Res 8:103–106
Schaffer WM, Zeh DW, Buchmann SL, Kleinhans S, Schaffer MV, Antrim J (1983) Competition for nectar between introduced honey bees and native North American bees and ants. Ecology 64:564–577
Shao ZY, Mao HX, Fu WJ, Ono M, Wang DS, Bonizzoni M, Zhang YP (2004) Genetic structure of Asian populations of Bombus ignitus. J Hered 95:46–52
Stolle E, Rohde M, Vautrin D, Solignac M, Schmid-Hempel P, Schmid Hempel R, Moritz RFA (2009) Novel microsatellite DNA loci for Bombus terrestris (Linnaeus, 1758). Mol Ecol 9:1345–1352
Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85:458–470
Tsuchida K, Kondo NI, Inoue MN, Goka K (2010) Reproductive disturbance risks to indigenous Japanese bumblebees from introduced Bombus terrestris. App Entomol Zool 45:49–58
Vähä J, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72
Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979
Wang J (2013) Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evol Int J Org Evol 67:3403–3411
Whittington R, Winston ML (2004) Comparison and examination of Bombus occidentalis and Bombus impatiens (Hymenoptera: Apidae) in tomato greenhouses. Econ Ent 97:1384–1389.
Winfree R et al (2007) Native bees provide insurance against ongoing honey bee losses. Ecol Lett 10:1105–1113
Winfree R, Aguilar R, Vazquez DP, Lebuhn G, Aizen MA (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076
Wolf S, Toev T, Moritz RL, Moritz RF (2012) Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae). Pop Ecol 54:115–124
Wright S (1951) The genetical structure of natural populations. Ann Eugen 15:323–354
Acknowledgements
We thank the numerous Cranberry growers who welcomed us into their agricultural areas for sampling, and the staff of the department of Environmental Conservation at the University of Massachusetts Amherst. This work was supported USDA-NIFA-SCRI Grant #2011-51181-30673, awarded to Anne Averill.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Suni, S.S., Scott, Z., Averill, A. et al. Population genetics of wild and managed pollinators: implications for crop pollination and the genetic integrity of wild bees. Conserv Genet 18, 667–677 (2017). https://doi.org/10.1007/s10592-017-0955-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-017-0955-5