in

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

  • 1.

    Sage, R. F. Global change biology: A primer. Glob. Change Biol. 26, 3–30 (2020).

    ADS 

    Google Scholar 

  • 2.

    Sutherland, W. J. et al. A horizon scan of emerging issues for global conservation in 2019. Trends Ecol. Evol. 34, 83–94 (2018).

    PubMed 

    Google Scholar 

  • 3.

    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).

    Google Scholar 

  • 4.

    Potts, S. G. et al. Safeguarding pollinators and their values to human well-being. Nature 540, 1–10 (2016).

    Google Scholar 

  • 5.

    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).

    PubMed 

    Google Scholar 

  • 6.

    Ellis, J. S. et al. Introgression in native populations of Apis mellifera mellifera L: implications for conservation. J. Insect Conserv. 22, 377–390 (2018).

    Google Scholar 

  • 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).

    Google Scholar 

  • 8.

    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).

    Google Scholar 

  • 9.

    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).

    PubMed 

    Google Scholar 

  • 10.

    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).

    Google Scholar 

  • 11.

    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).

    Google Scholar 

  • 12.

    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).

    Google Scholar 

  • 13.

    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).

    Google Scholar 

  • 14.

    Martinet, B. et al. Global effects of extreme temperatures on wild bumblebees. Conserv. Biol. 35(5), 1507–1518 (2021).

    PubMed 

    Google Scholar 

  • 15.

    Schmid-Hempel, R. et al. The invasion of southern South America by imported bumblebees and associated parasites. J. Anim. Ecol. 83, 823–837 (2014).

    PubMed 

    Google Scholar 

  • 16.

    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).

    Google Scholar 

  • 17.

    Tsuchida, K., Yamaguchi, A., Kanbe, Y. & Goka, K. Reproductive interference in an introduced bumblebee: Polyandry may mitigate negative reproductive impact. Insects 10, 59 (2019).

    PubMed Central 

    Google Scholar 

  • 18.

    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).

    Google Scholar 

  • 19.

    Lecocq, T. et al. The alien’s identity: Consequences of taxonomic status for the international bumblebee trade regulations. Biol. Conserv. 195, 169–176 (2016).

    Google Scholar 

  • 20.

    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).

    Google Scholar 

  • 21.

    Hewitt, G. M. Mediterranean Peninsulas: The Evolution of Hotspots. In Biodiversity Hotspots (eds Zachos, F. & Habel, J.) 123–147 (Springer-Verlag, 2011).

    Google Scholar 

  • 22.

    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).

    Google Scholar 

  • 23.

    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).

    CAS 
    PubMed 

    Google Scholar 

  • 24.

    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).

    Google Scholar 

  • 25.

    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).

    Google Scholar 

  • 26.

    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).

    Google Scholar 

  • 27.

    Williams, P. H. et al. Genes suggest ancestral colour polymorphisms are shared across morphologically cryptic species in arctic bumblebees. PLoS ONE 10, e0144544 (2015).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 28.

    Gosterit, A. Adverse effects of inbreeding on colony foundation success in bumblebees, Bombus terrestris (Hymenoptera: Apidae). Appl. Entomol. Zool. 51, 521–526 (2016).

    Google Scholar 

  • 29.

    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).

    CAS 

    Google Scholar 

  • 30.

    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).

    CAS 

    Google Scholar 

  • 31.

    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).

    CAS 
    PubMed 

    Google Scholar 

  • 32.

    Gosterit, A. & Baskar, V. C. Impacts of commercialization on the developmental characteristics of native Bombus terrestris (L.) colonies. Insectes Soc. 63, 609–614 (2016).

    Google Scholar 

  • 33.

    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).

    PubMed 

    Google Scholar 

  • 34.

    Zayed, A. Bee genetics and conservation. Apidologie 40, 237–262 (2009).

    Google Scholar 

  • 35.

    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).

    Google Scholar 

  • 36.

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

    PubMed 
    PubMed Central 

    Google Scholar 

  • 37.

    Bogo, G. et al. No evidence for an inbreeding avoidance system in the bumble bee Bombus terrestris. Apidologie 49, 473–483 (2018).

    Google Scholar 

  • 38.

    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).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 39.

    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).

    Google Scholar 

  • 40.

    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).

  • 41.

    Nei, M. Genetic distance between populations. Am. Nat. 106, 283–292 (1972).

    Google Scholar 

  • 42.

    Rannala, B. & Mountain, J. L. Detecting immigration by using multilocus genotypes. PNAS 94, 9197–9201 (1997).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 43.

    Anderson, E. C. Bayesian inference of species hybrids using multilocus dominant genetic markers. Philos. Trans. R. Soc. B 363(1505), 2841–2850 (2008).

    Google Scholar 

  • 44.

    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).

    Google Scholar 

  • 45.

    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).

    PubMed 

    Google Scholar 

  • 46.

    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).

    Google Scholar 

  • 47.

    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).

    Google Scholar 

  • 48.

    Arnold, M. L. & Kunte, K. Adaptive genetic exchange: A tangled history of admixture and evolutionary innovation. Trends Ecol. Evol. 32, 601–611 (2017).

    PubMed 

    Google Scholar 

  • 49.

    Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237 (2005).

    PubMed 

    Google Scholar 

  • 50.

    De la Rúa, P. et al. Conserving genetic diversity in the honeybee: Comments on Harpur et al. (2012). Mol. Ecol. 22, 3208–3210 (2013).

    PubMed 

    Google Scholar 

  • 51.

    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).

    CAS 
    PubMed 

    Google Scholar 

  • 52.

    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).

    Google Scholar 

  • 53.

    Ayabe, T., Hoshiba, H. & Ono, M. Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris. Chromosome Res. 12, 215–223 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • 54.

    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).

    Google Scholar 

  • 55.

    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).

    CAS 
    PubMed 

    Google Scholar 

  • 56.

    Gerloff, C. U. & Schmid-Hempel, P. Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos 111, 67–80 (2005).

    Google Scholar 

  • 57.

    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).

    CAS 
    PubMed 

    Google Scholar 

  • 58.

    Ivanova, N., Dewaard, J. & Herbert, D. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol. Ecol. Notes 6, 998–1002 (2006).

    CAS 

    Google Scholar 

  • 59.

    Wandeler, P., Hoeck, P. E. & Keller, L. F. Back to the future: museum specimens in population genetics. Trends Ecol. Evol. 22, 634–642 (2007).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 60.

    Rozen, S. & Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers. Bioinform. Methods Protoc. 132, 365–386 (2000).

    CAS 

    Google Scholar 

  • 61.

    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).

    CAS 

    Google Scholar 

  • 62.

    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).

    CAS 
    PubMed 

    Google Scholar 

  • 63.

    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).

    Google Scholar 

  • 64.

    Wang, J. Computationally efficent sibship and parentage assignment from multilocus marker data. Genetics 191, 183–194 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 65.

    Piry, S. et al. Geneclass2: A software for genetic assignment and first generation migrant detection. Heredity 95(6), 536–539 (2004).

    CAS 

    Google Scholar 

  • 66.

    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).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    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).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 68.

    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).

    Google Scholar 

  • 69.

    Rousset, F. genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106 (2008).

    PubMed 

    Google Scholar 

  • 70.

    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).

    CAS 

    Google Scholar 

  • 71.

    Goudet, J. FSTAT (version 1.2): A computer program to calculate F-statistics. J. Hered. 86, 485–486 (1995).

    Google Scholar 

  • 72.

    R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, http://www.R-project.org (2008).

  • 73.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 74.

    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).

    CAS 
    PubMed 

    Google Scholar 

  • 75.

    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).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 76.

    Rosenberg, N. A. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138 (2004).

    Google Scholar 

  • 77.

    Jombart, T. & Ahmed, I. adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics 24, 1403–1405 (2011).

    Google Scholar 


  • Source: Ecology - nature.com

    At UN climate change conference, trying to “keep 1.5 alive”

    Direct and indirect effects of roads on space use by jaguars in Brazil