Spatial and temporal patterns of genetic diversity in Bombus terrestris populations of the Iberian Peninsula and their conservation implications.

Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE

Original Publication: London : Nature Publishing Group, copyright 2011-

Genetic Variation*; Bees/*physiology; Alleles ; Animals ; Biodiversity ; Cluster Analysis ; Conservation of Natural Resources ; DNA, Mitochondrial/metabolism ; Female ; Genetics, Population ; Genotype ; Geography ; Haplotypes ; Male ; Mitochondria/metabolism ; Nucleic Acid Hybridization ; Pollination ; Population Dynamics ; Principal Component Analysis ; Spain ; Time Factors

The bumblebee Bombus terrestris is used worldwide for crop pollination. Despite its positive impact on crop yield, it has become a widespread threat to biodiversity due to its interactions with local bumblebee populations. Commercial subspecies introduced to the Iberian Peninsula since the 1990s without any regulation have colonized the environment, with evidence of naturalization and introgression with the endemic subspecies Bombus terrestris lusitanicus. We have used mitochondrial and nuclear genetic data to describe the current genetic diversity of the Iberian population and to estimate the expansion of commercial bumblebees. Samples from the natural distribution range of the commercial subspecies, the natural intergradation area between the two subspecies and from a period prior to the use of commercial colonies (i.e., before the 1990s) have been used for comparison. Our results show that the mitochondrial haplotype of the commercial breeds has spread throughout the territory, which, together with subtle changes observed in the nuclear genetic diversity of the populations, indicates that hybridization and consequent introgression are occurring in most of the peninsula. It is, therefore, necessary to improve the existing legislation concerning the management and exportation of commercial bumblebees to conserve locally adapted populations.
(© 2021. The Author(s).)

Sage, R. F. Global change biology: A primer. Glob. Change Biol. 26, 3–30 (2020). (PMID: 10.1111/gcb.14893)
Sutherland, W. J. et al. A horizon scan of emerging issues for global conservation in 2019. Trends Ecol. Evol. 34, 83–94 (2018). (PMID: 3055480810.1016/j.tree.2018.11.001)
Porto, R. G. et al. Pollination ecosystem services: A comprehensive review of economic values, research funding and policy actions. Food Secur. 12, 1425–1442 (2020). (PMID: 10.1007/s12571-020-01043-w)
Potts, S. G. et al. Safeguarding pollinators and their values to human well-being. Nature 540, 1–10 (2016). (PMID: 10.1038/nature20588)
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015). (PMID: 2572150610.1126/science.1255957)
Ellis, J. S. et al. Introgression in native populations of Apis mellifera mellifera L: implications for conservation. J. Insect Conserv. 22, 377–390 (2018). (PMID: 10.1007/s10841-018-0067-7)
Hart, A. F., Maebe, K., Brown, G., Smagghe, G. & Ings, T. Winter activity unrelated to introgression in British bumblebee Bombus terrestris audax. Apidologie 52, 315–327 (2021). (PMID: 10.1007/s13592-020-00822-w)
Ings, T. C., Ward, N. L. & Chittka, L. Can commercially imported bumble bees out-compete their native conspecifics?. J. Appl. Ecol. 43, 940–948 (2006). (PMID: 10.1111/j.1365-2664.2006.01199.x)
Graystock, P., Blane, E. J., McFrederick, Q. S., Goulson, D. & Hughes, W. O. Do managed bees drive parasite spread and emergence in wild bees?. IJP-PAW 5, 64–75 (2016). (PMID: 28560161)
Chandler, D., Cooper, E. & Prince, G. Are there risks to wild European bumble bees from using commercial stocks of domesticated Bombus terrestris for crop pollination?. J. Apic. Res. 58, 1–17 (2019). (PMID: 10.1080/00218839.2019.1637238)
Velthuis, H. H. W. & Doorn, A. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37, 421–451 (2006). (PMID: 10.1051/apido:2006019)
Trillo, A. et al. Contrasting occurrence patterns of managed and native bumblebees in natural habitats across a greenhouse landscape gradient. Agric. Ecosyst. Environ. 272, 230–236 (2019). (PMID: 10.1016/j.agee.2018.11.018)
Lecocq, T., Rasmont, P., Harpke, A. & Schweiger, O. Improving international trade regulation by considering intraspecific variation for invasion risk assessment of commercially traded species: The Bombus terrestris case. Conserv. Lett. 9, 281–289 (2015). (PMID: 10.1111/conl.12215)
Martinet, B. et al. Global effects of extreme temperatures on wild bumblebees. Conserv. Biol. 35(5), 1507–1518 (2021). (PMID: 3331936810.1111/cobi.13685)
Schmid-Hempel, R. et al. The invasion of southern South America by imported bumblebees and associated parasites. J. Anim. Ecol. 83, 823–837 (2014). (PMID: 2425642910.1111/1365-2656.12185)
Aizen, M. A. et al. Coordinated species importation policies are needed to reduce serious invasions globally: The case of alien bumblebees in South America. J. Appl. Ecol. 56, 100–106 (2018). (PMID: 10.1111/1365-2664.13121)
Tsuchida, K., Yamaguchi, A., Kanbe, Y. & Goka, K. Reproductive interference in an introduced bumblebee: Polyandry may mitigate negative reproductive impact. Insects 10, 59 (2019). (PMID: 640960510.3390/insects10020059)
Rasmont, P., Coppée, A., Michez, D. & De Meulemeester, T. An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae). Ann. Soc. Entomol. Fr. (N.S.) 44, 243–250 (2008). (PMID: 10.1080/00379271.2008.10697559)
Lecocq, T. et al. The alien’s identity: Consequences of taxonomic status for the international bumblebee trade regulations. Biol. Conserv. 195, 169–176 (2016). (PMID: 10.1016/j.biocon.2016.01.004)
Ornosa, C. & Ortiz-Sánchez, F. Hymenoptera: Apoidea I. In Fauna Ibérica Vol. 23 (eds Ramos, M. A. et al.) (Museo Nacional de Ciencias Naturales, CSIC, 2004).
Hewitt, G. M. Mediterranean Peninsulas: The Evolution of Hotspots. In Biodiversity Hotspots (eds Zachos, F. & Habel, J.) 123–147 (Springer-Verlag, 2011). (PMID: 10.1007/978-3-642-20992-5_7)
Ortiz-Sánchez, F. Introducción de Bombus terrestris terrestris (Linnaeus, 1758) en el Sur de España para la polinización de cultivos en invernadero (Hymenoptera, Apidae). Boln. Asoc. Esp. Ent. 16, 247–248 (1992).
Cejas, D., López-López, A., Muñoz, I., Ornosa, C. & De la Rúa, P. Unveiling introgression in bumblebee (Bombus terrestris) populations through mitogenome-based markers. Anim. Genet. 51, 70–77 (2020). (PMID: 3164838010.1111/age.12874)
Seabra, S. G. et al. Genomic signatures of introgression between commercial and native bumblebees, Bombus terrestris, in western Iberian Peninsula—Implications for conservation and trade regulation. Evol. Appl. 12, 1–13 (2019). (PMID: 10.1111/eva.12732)
Bartomeus, I., Molina, F. P., Hidalgo-Galiana, A. & Ortego, J. Safeguarding the genetic integrity of native pollinators requires stronger regulations on commercial lines. Ecol. Solut. Evid. 1(1), e12012 (2020). (PMID: 10.1002/2688-8319.12012)
Coates, D. J., Byrne, M. & Moritz, C. Genetic diversity and conservation units: Dealing with the species-population continuum in the age of genomics. Front. Ecol. Evol. 6, 165 (2018). (PMID: 10.3389/fevo.2018.00165)
Williams, P. H. et al. Genes suggest ancestral colour polymorphisms are shared across morphologically cryptic species in arctic bumblebees. PLoS ONE 10, e0144544 (2015). (PMID: 26657658468434310.1371/journal.pone.0144544)
Gosterit, A. Adverse effects of inbreeding on colony foundation success in bumblebees, Bombus terrestris (Hymenoptera: Apidae). Appl. Entomol. Zool. 51, 521–526 (2016). (PMID: 10.1007/s13355-016-0427-2)
Maebe, K., Karise, R., Meeus, I., Mänd, M. & Smagghe, G. Pattern of population structuring between Belgian and Estonian bumblebees. Sci. Rep. 9, 1–8 (2019). (PMID: 10.1038/s41598-019-46188-7)
Allio, R., Donega, S., Galtier, N. & Nabholz, B. Large variation in the ratio of mitochondrial to nuclear mutation rate across animals: Implications for genetic diversity and the use of mitochondrial DNA as a molecular marker. Mol. Biol. Evol. 34, 2762–2772 (2017). (PMID: 2898172110.1093/molbev/msx197)
Patten, M. M., Carioscia, S. A. & Linnen, C. R. Biased introgression of mitochondrial and nuclear genes: A comparison of diploid and haplodiploid systems. Mol. Ecol. 24, 5200–5210 (2015). (PMID: 2617346910.1111/mec.13318)
Gosterit, A. & Baskar, V. C. Impacts of commercialization on the developmental characteristics of native Bombus terrestris (L.) colonies. Insectes Soc. 63, 609–614 (2016). (PMID: 10.1007/s00040-016-0507-x)
Moreira, A. S., Horgan, F. G., Murray, T. E. & Kakouli-Duarte, T. Population genetic structure of Bombus terrestris in Europe: Isolation and genetic differentiation of Irish and British populations. Mol. Ecol. 24, 3257–3268 (2015). (PMID: 2595897710.1111/mec.13235)
Zayed, A. Bee genetics and conservation. Apidologie 40, 237–262 (2009). (PMID: 10.1051/apido/2009026)
Schenau, E. & Jha, S. High levels of male diploidy but low levels of genetic structure characterize Bombus vosnesenskii populations across the Western US. Conserv. Genet. 18, 597–605 (2017). (PMID: 10.1007/s10592-016-0900-z)
Van Wilgenburg, E., Driessen, G. & Beukeboom, L. W. Single locus complementary sex determination in Hymenoptera: An “unintelligent” design?. Front. Zool. 3, 1–15 (2006). (PMID: 16393347136007210.1186/1742-9994-3-1)
Bogo, G. et al. No evidence for an inbreeding avoidance system in the bumble bee Bombus terrestris. Apidologie 49, 473–483 (2018). (PMID: 10.1007/s13592-018-0575-1)
Kent, C. F. et al. Conservation genomics of the declining North American bumblebee Bombus terricola reveals inbreeding and selection on immune genes. Front. Genet. 9, 316 (2018). (PMID: 30147708609597510.3389/fgene.2018.00316)
Cejas, D., Ornosa, C., Muñoz, I. & De la Rúa, P. Searching for molecular markers to differentiate Bombus terrestris (Linnaeus) subspecies in the Iberian Peninsula. Sociobiology 65, 558–565 (2018). (PMID: 10.13102/sociobiology.v65i4.3442)
Ministerio de Agricultura, Pesca y Alimentación de España. Encuesta sobre Superficies y Rendimientos de Cultivos (ESYRCE). https://cpage.mpr.gob.es N.I.P.O.: 001-19-051-9 (2021).
Nei, M. Genetic distance between populations. Am. Nat. 106, 283–292 (1972). (PMID: 10.1086/282771)
Rannala, B. & Mountain, J. L. Detecting immigration by using multilocus genotypes. PNAS 94, 9197–9201 (1997). (PMID: 92564592311110.1073/pnas.94.17.9197)
Anderson, E. C. Bayesian inference of species hybrids using multilocus dominant genetic markers. Philos. Trans. R. Soc. B 363(1505), 2841–2850 (2008). (PMID: 10.1098/rstb.2008.0043)
Earl, D. A. & von Holdt, B. M. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012). (PMID: 10.1007/s12686-011-9548-7)
Facon, B. et al. Can things get worse when an invasive species hybridizes? The harlequin ladybird Harmonia axyridis in France as a case study. Evol. Appl. 4, 71–88 (2011). (PMID: 2556795410.1111/j.1752-4571.2010.00134.x)
Ornosa, C., Torres, F. & De la Rúa, P. Updated list of bumblebees (Hymenoptera: Apidae) from the Spanish Pyrenees with notes on their decline and conservation status. Zootaxa 4237, 41–77 (2017). (PMID: 10.11646/zootaxa.4237.1.3)
Allendorf, F. W., Leary, R. F., Spruell, P. & Wenburg, J. K. The problems with hybrids: Setting conservation guidelines. Trends Ecol. Evol. 16, 613–622 (2001). (PMID: 10.1016/S0169-5347(01)02290-X)
Arnold, M. L. & Kunte, K. Adaptive genetic exchange: A tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32, 601–611 (2017). (PMID: 2864548610.1016/j.tree.2017.05.007)
Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237 (2005). (PMID: 1670137410.1016/j.tree.2005.02.010)
De la Rúa, P. et al. Conserving genetic diversity in the honeybee: Comments on Harpur et al. (2012). Mol. Ecol. 22, 3208–3210 (2013). (PMID: 2443357210.1111/mec.12333)
Estoup, A., Solignac, M., Cornuet, J. M., Goudet, J. & Scholl, A. Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol. Ecol. 5, 19–31 (1996). (PMID: 914769310.1111/j.1365-294X.1996.tb00288.x)
Silva, S. E. et al. Population genomics of Bombus terrestris reveals high but unstructured genetic diversity in a potential glacial refugium. Biol. J. Linn. Soc. 129, 259–272 (2020). (PMID: 10.1093/biolinnean/blz182)
Ayabe, T., Hoshiba, H. & Ono, M. Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris. Chromosome Res. 12, 215–223 (2004). (PMID: 1512563510.1023/B:CHRO.0000021880.83639.4b)
Takahashi, J., Ayabe, T., Mitsuhata, M., Shimizu, I. & Ono, M. Diploid male production in a rare and locally distributed bumblebee, Bombus florilegus (Hymenoptera, Apidae). Insectes Soc. 55, 43–50 (2008). (PMID: 10.1007/s00040-007-0976-z)
Darvill, B., Ellis, J. S., Lye, G. C. & Goulson, D. Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol. Ecol. 15, 601–611 (2006). (PMID: 1649968810.1111/j.1365-294X.2006.02797.x)
Gerloff, C. U. & Schmid-Hempel, P. Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos 111, 67–80 (2005). (PMID: 10.1111/j.0030-1299.2005.13980.x)
Kraus, F. B., Wolf, S. & Moritz, R. F. A. Male flight distance and population substructure in the bumblebee Bombus terrestris. J. Anim. Ecol. 78, 247–252 (2009). (PMID: 1912060510.1111/j.1365-2656.2008.01479.x)
Ivanova, N., Dewaard, J. & Herbert, D. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol. Ecol. Notes 6, 998–1002 (2006). (PMID: 10.1111/j.1471-8286.2006.01428.x)
Wandeler, P., Hoeck, P. E. & Keller, L. F. Back to the future: museum specimens in population genetics. Trends Ecol. Evol. 22, 634–642 (2007). (PMID: 1798875810.1016/j.tree.2007.08.017)
Rozen, S. & Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers. Bioinform. Methods Protoc. 132, 365–386 (2000). (PMID: 10.1385/1-59259-192-2:365)
Hines, H., Cameron, S. & Williams, P. Molecular phylogeny of the bumble bee subgenus Pyrobombus (Hymenoptera: Apidae: Bombus) with insights into gene utility for lower-level analysis. Invertebr. Syst. 20, 289–303 (2006). (PMID: 10.1071/IS05028)
Estoup, A., Scholl, A., Pouvreau, A. & Solignac, M. Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol. Ecol. 4, 89–94 (1995). (PMID: 771195710.1111/j.1365-294X.1995.tb00195.x)
Cejas, D., Ornosa, C., Muñoz, I. & De la Rúa, P. Preliminary report on cross-species microsatellite amplification for bumblebee biodiversity and conservation studies. Arch. de Zootec. 68, 422–426 (2019).
Wang, J. Computationally efficent sibship and parentage assignment from multilocus marker data. Genetics 191, 183–194 (2012). (PMID: 22367033333825910.1534/genetics.111.138149)
Piry, S. et al. Geneclass2: A software for genetic assignment and first generation migrant detection. Heredity 95(6), 536–539 (2004). (PMID: 10.1093/jhered/esh074)
Cornuet, J. M., Piry, S., Luikart, G., Estoup, A. & Solignac, M. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153, 1989–2000 (1999). (PMID: 10581301146084310.1093/genetics/153.4.1989)
Peakall, R. & Smouse, P. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—An update. Bioinformatics 28, 2537–2539 (2012). (PMID: 22820204346324510.1093/bioinformatics/bts460)
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. & Shipley, P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538 (2004). (PMID: 10.1111/j.1471-8286.2004.00684.x)
Rousset, F. genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106 (2008). (PMID: 2158572710.1111/j.1471-8286.2007.01931.x)
Kalinowski, S. T. HP-RARE 1.0: A computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 5, 187–189 (2005). (PMID: 10.1111/j.1471-8286.2004.00845.x)
Goudet, J. FSTAT (version 1.2): A computer program to calculate F-statistics. J. Hered. 86, 485–486 (1995). (PMID: 10.1093/oxfordjournals.jhered.a111627)
R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, http://www.R-project.org (2008).
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000). (PMID: 10835412146109610.1093/genetics/155.2.945)
Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol. Ecol. 14, 2611–2620 (2005). (PMID: 1596973910.1111/j.1365-294X.2005.02553.x)
Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A. & Mayrose, I. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 15, 1179–1191 (2015). (PMID: 25684545453433510.1111/1755-0998.12387)
Rosenberg, N. A. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138 (2004). (PMID: 10.1046/j.1471-8286.2003.00566.x)
Jombart, T. & Ahmed, I. adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics 24, 1403–1405 (2011). (PMID: 10.1093/bioinformatics/btn129)

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