in

Urban ecosystem drives genetic diversity in feral honey bee

  • United Nations, Department of Economic and Social Affairs & Population Division. World Urbanization Prospects: The 2018 Revision (ST/ESA/SER.A/420). (United Nations, 2019).

  • Wei, Y. D. & Ewing, R. Urban expansion, sprawl and inequality. Landsc. Urban Plan. 177, 259–265. https://doi.org/10.1016/j.landurbplan.2018.05.021 (2018).

    Article 

    Google Scholar 

  • Ayers, A. C. & Rehan, S. M. Supporting bees in cities: How bees are influenced by local and landscape features. Insects 12 (2021).

  • Grimm, N. B. et al. Global change and the ecology of cities. Science 319, 756–760. https://doi.org/10.1126/science.1150195 (2008).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419 (2003).

    Article 

    Google Scholar 

  • Shochat, E. et al. Invasion, competition, and biodiversity loss in urban ecosystems. Bioscience 60, 199–208. https://doi.org/10.1525/bio.2010.60.3.6 (2010).

    Article 

    Google Scholar 

  • Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: A review of its drivers. Biol. Cons. 232, 8–27. https://doi.org/10.1016/j.biocon.2019.01.020 (2019).

    Article 

    Google Scholar 

  • Seibold, S. et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674. https://doi.org/10.1038/s41586-019-1684-3 (2019).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Wagner, D. L. Insect declines in the anthropocene. Annu. Rev. Entomol. 65, 457–480. https://doi.org/10.1146/annurev-ento-011019-025151 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Brown, M. J. & Paxton, R. J. The conservation of bees: A global perspective. Apidologie 40, 410–416 (2009).

    Google Scholar 

  • Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kennedy, C. M. et al. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599 (2013).

    PubMed 

    Google Scholar 

  • Potts, S. G. et al. Summary for policymakers of the assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. (2016).

  • Winfree, R., Aguilar, R., Vázquez, D. P., LeBuhn, G. & Aizen, M. A. A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076 (2009).

    PubMed 

    Google Scholar 

  • Millard, J. et al. Global effects of land-use intensity on local pollinator biodiversity. Nat. Commun. 12, 1–11 (2021).

    ADS 

    Google Scholar 

  • Baldock, K. C. et al. A systems approach reveals urban pollinator hotspots and conservation opportunities. Nat. Ecol. Evolut. 3, 363–373 (2019).

    Google Scholar 

  • Banaszak-Cibicka, W., Twerd, L., Fliszkiewicz, M., Giejdasz, K. & Langowska, A. City parks vs. natural areas—Is it possible to preserve a natural level of bee richness and abundance in a city park?. Urban Ecosyst. 21, 599–613 (2018).

    Google Scholar 

  • Hall, D. M. et al. The city as a refuge for insect pollinators. Conserv. Biol. 31, 24–29 (2017).

    PubMed 

    Google Scholar 

  • Theodorou, P. et al. Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nat. Commun. 11, 1–13 (2020).

    Google Scholar 

  • Wilson, C. J. & Jamieson, M. A. The effects of urbanization on bee communities depends on floral resource availability and bee functional traits. PLoS ONE 14, e0225852 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Samuelson, A. E., Schürch, R. & Leadbeater, E. Dancing bees evaluate central urban forage resources as superior to agricultural land. J. Appl. Ecol. 59, 79–88 (2022).

    Google Scholar 

  • Fortel, L. et al. Decreasing abundance, increasing diversity and changing structure of the wild bee community (Hymenoptera: Anthophila) along an urbanization gradient. PLoS ONE 9, e104679 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Roffet-Salque, M. et al. Widespread exploitation of the honeybee by early Neolithic farmers. Nature 527, 226–230 (2015).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Crane, E. Recent research on the world history of beekeeping. Bee World 80, 174–186 (1999).

    Google Scholar 

  • Dietemann, V., Pirk, C. W. W. & Crewe, R. Is there a need for conservation of honeybees in Africa?. Apidologie 40, 285–295 (2009).

    Google Scholar 

  • Jaffe, R. et al. Estimating the density of honeybee colonies across their natural range to fill the gap in pollinator decline censuses. Conserv. Biol. 24, 583–593 (2010).

    PubMed 

    Google Scholar 

  • Browne, K. A. et al. Investigation of free-living honey bee colonies in Ireland. J. Apic. Res. 60, 229–240. https://doi.org/10.1080/00218839.2020.1837530 (2021).

    Article 

    Google Scholar 

  • Kohl, P. L. & Rutschmann, B. The neglected bee trees: European beech forests as a home for feral honey bee colonies. PeerJ 6, e4602 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Oleksa, A., Gawroński, R. & Tofilski, A. Rural avenues as a refuge for feral honey bee population. J. Insect Conserv. 17, 465–472 (2013).

    Google Scholar 

  • Rutschmann, B., Kohl, P. L., Machado, A. & Steffan-Dewenter, I. Semi-natural habitats promote winter survival of wild-living honeybees in an agricultural landscape. Biol. Cons. 266, 109450 (2022).

    Google Scholar 

  • Thompson, C. E., Biesmeijer, J. C., Allnutt, T. R., Pietravalle, S. & Budge, G. E. Parasite pressures on feral honey bees (Apis mellifera sp). PLoS ONE 9, e105164 (2014).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bila Dubaić, J. et al. Unprecedented density and persistence of feral honey bees in urban environments of a large SE-European City (Belgrade, Serbia). Insects 12, 1127 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Alaux, C., Le Conte, Y. & Decourtye, A. Pitting wild bees against managed honey bees in their native range, a losing strategy for the conservation of honey bee biodiversity. Front. Ecol. Evol. 7, 60 (2019).

    Google Scholar 

  • Requier, F. et al. The conservation of native honey bees is crucial. Trends Ecol. Evol. 34, 789–798 (2019).

    PubMed 

    Google Scholar 

  • Mladenović, S. et al. Environment in Belgrade in 2018. (in Serbian: Kvalitet životne sredine u Beogradu u 2018. godini). (The City Administration, Secretariat for Environmental Protection, 2019).

  • Statistical Office of the Republic of Serbia. https://data.stat.gov.rs/Home/Result/130202010207?languageCode=en-US.

  • (“The Official Gazette of the Republic of Serbia”, Nos. 41/2009, 93/2012 and 14/2106 [In Serbian], 2009).

  • Johnson, M. T. & Munshi-South, J. Evolution of life in urban environments. Science 358, eaam8327 (2017).

    PubMed 

    Google Scholar 

  • Jara, L. et al. Stable genetic diversity despite parasite and pathogen spread in honey bee colonies. Sci. Nat. 102, 1–8 (2015).

    Google Scholar 

  • Tanasković, M. et al. MtDNA analysis indicates human-induced temporal changes of serbian honey bees diversity. Insects 12, 767 (2021).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Wang, J. COANCESTRY: A program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol. Ecol. Resour. 11, 141–145. https://doi.org/10.1111/j.1755-0998.2010.02885.x (2011).

    Article 
    PubMed 

    Google Scholar 

  • Wang, J. Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet. Res. 89, 135–153. https://doi.org/10.1017/s0016672307008798 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Jacobson, S. Locally adapted, varroa resistant honey bees: ideas from several key studies. Am. Bee J. (2010).

  • McNeely, J. A., Miller, K. R., Reid, W. V., Mettermeier, R. A. & Werner, T. B. Conserving the world’s biological diversity. (UICN, Morges (Suiza) WRI, Washington DC (EUA) CI, Washington DC (EUA) WWF …, 1990).

  • Hoban, S. M. et al. Bringing genetic diversity to the forefront of conservation policy and management. Conserv. Genet. Resour. 5, 593–598 (2013).

    Google Scholar 

  • Hohenlohe, P. A., Funk, W. C. & Rajora, O. P. Population genomics for wildlife conservation and management. Mol. Ecol. 30, 62–82 (2021).

    PubMed 

    Google Scholar 

  • Shafer, A. B. et al. Genomics and the challenging translation into conservation practice. Trends Ecol. Evol. 30, 78–87 (2015).

    PubMed 

    Google Scholar 

  • Mattila, H. R. & Seeley, T. D. Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317, 362–364 (2007).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Oddie, M. A. & Dahle, B. Insights from Norway: Using natural adaptation to breed Varroa-resistant honey bees. Bee World 98, 38–43 (2021).

    Google Scholar 

  • Oddie, M. A., Dahle, B. & Neumann, P. Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection. PeerJ 5, e3956 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Oldroyd, B. P. & Fewell, J. H. Genetic diversity promotes homeostasis in insect colonies. Trends Ecol. Evol. 22, 408–413 (2007).

    PubMed 

    Google Scholar 

  • Tarpy, D. R. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R Soc. Lond. Series B Biol. Sci. 270, 99–103 (2003).

    Google Scholar 

  • van Baalen, M. & Beekman, M. The costs and benefits of genetic heterogeneity in resistance against parasites in social insects. Am. Nat. 167, 568–577 (2006).

    PubMed 

    Google Scholar 

  • Eckholm, B. J., Anderson, K. E., Weiss, M. & DeGrandi-Hoffman, G. Intracolonial genetic diversity in honeybee (Apis mellifera) colonies increases pollen foraging efficiency. Behav. Ecol. Sociobiol. 65, 1037–1044 (2011).

    Google Scholar 

  • Graham, S., Myerscough, M., Jones, J. & Oldroyd, B. Modelling the role of intracolonial genetic diversity on regulation of brood temperature in honey bee (Apis mellifera L.) colonies. Insectes Soc. 53, 226–232 (2006).

    Google Scholar 

  • Jones, J. C., Myerscough, M. R., Graham, S. & Oldroyd, B. P. Honey bee nest thermoregulation: Diversity promotes stability. Science 305, 402–404 (2004).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Tanasković, M. et al. Further evidence of population admixture in the Serbian honey bee population. Insects 13, 180 (2022).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Nedić, N. et al. Detecting population admixture in honey bees of Serbia. J. Apic. Res. 53, 303–313. https://doi.org/10.3896/IBRA.1.53.2.12 (2014).

    Article 

    Google Scholar 

  • Nedić, N., Stanisavljević, L., Mladenović, M. & Stanisavljević, J. Molecular characterization of the honeybee Apis mellifera carnica in Serbia. Arch. Biol. Sci. 61, 587–598 (2009).

    Google Scholar 

  • Kükrer, M., Kence, M. & Kence, A. Honey bee diversity is swayed by migratory beekeeping and trade despite conservation practices: Genetic evidence for the impact of anthropogenic factors on population structure. Front. Ecol. Evolut. 9 (2021).

  • Bouga, M., Harizanis, P. C., Kilias, G. & Alahiotis, S. Genetic divergence and phylogenetic relationships of honey bee Apis mellifera (Hymenoptera: Apidae) populations from Greece and Cyprus using PCR–RFLP analysis of three mtDNA segments. Apidologie 36, 335–344 (2005).

    CAS 

    Google Scholar 

  • Dall’Olio, R., Marino, A., Lodesani, M. & Moritz, R. F. Genetic characterization of Italian honeybees, Apis mellifera ligustica, based on microsatellite DNA polymorphisms. Apidologie 38, 207–217 (2007).

    CAS 

    Google Scholar 

  • Neumann, P. & Blacquière, T. The Darwin cure for apiculture? Natural selection and managed honeybee health. Evol. Appl. 10, 226–230 (2017).

    PubMed 

    Google Scholar 

  • Kulinčević, J., Rinderer, T., Mladjan, V. & Buco, S. Five years of bi-directional genetic selection for honey bees resistant and susceptible to Varroa jacobsoni. Apidologie 23, 443–452 (1992).

    Google Scholar 

  • 2011 Census of Population, Households and Dwellings in the Republic of Serbia: Comparative Overview of the Number of Population in 1948, 1953, 1961, 1971, 1981, 1991, 2002 and 2011. (Statistical Office of the Republic of Serbia, 2014).

  • Techer, M. A. et al. Large-scale mitochondrial DNA analysis of native honey bee Apis mellifera populations reveals a new African subgroup private to the South West Indian Ocean islands. BMC Genet. 18, 1–21 (2017).

    Google Scholar 

  • Garnery, L., Cornuet, J. M. & Solignac, M. Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Mol. Ecol. 1, 145–154 (1992).

    CAS 
    PubMed 

    Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resources. 10, 564–567 (2010).

    Google Scholar 

  • 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 

  • Stoneking, M., Hedgecock, D., Higuchi, R. G., Vigilant, L. & Erlich, H. A. Population variation of human mtDNA control region sequences detected by enzymatic amplification and sequence-specific oligonucleotide probes. Am. J. Hum. Genet. 48, 370 (1991).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hammer, Ø., Harper, D. A. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 9 (2001).

    Google Scholar 

  • Crozier, R. & Crozier, Y. The mitochondrial genome of the honeybee Apis mellifera: Complete sequence and genome organization. Genetics 133, 97–117 (1993).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Falush, D., Stephens, M. & Pritchard, J. K. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164, 1567–1587. https://doi.org/10.1093/genetics/164.4.1567 (2003).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Falush, D., Stephens, M. & Pritchard, J. K. Inference of population structure using multilocus genotype data: Dominant markers and null alleles. Mol. Ecol. Notes 7, 574–578 (2007).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hubisz, M. J., Falush, D., Stephens, M. & Pritchard, J. K. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9, 1322–1332. https://doi.org/10.1111/j.1755-0998.2009.02591.x (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 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 

  • Earl, D. A. & VonHoldt, 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 

  • 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 

  • Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94. https://doi.org/10.1186/1471-2156-11-94 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ward, J. H. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236–244. https://doi.org/10.1080/01621459.1963.10500845 (1963).

    Article 
    MathSciNet 

    Google Scholar 

  • Wang, J. An estimator for pairwise relatedness using molecular markers. Genetics 160, 1203–1215. https://doi.org/10.1093/genetics/160.3.1203 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, C. C., Weeks, D. E. & Chakravarti, A. Similarity of DNA fingerprints due to chance and relatedness. Hum. Hered. 43, 45–52. https://doi.org/10.1159/000154113 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lynch, M. Estimation of relatedness by DNA fingerprinting. Mol. Biol. Evol. 5, 584–599. https://doi.org/10.1093/oxfordjournals.molbev.a040518 (1988).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lynch, M. & Ritland, K. Estimation of pairwise relatedness with molecular markers. Genetics 152, 1753–1766. https://doi.org/10.1093/genetics/152.4.1753 (1999).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ritland, K. Estimators for pairwise relatedness and individual inbreeding coefficients. Genet. Res. 67, 175–185 (1996).

    Google Scholar 

  • Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275. https://doi.org/10.1111/j.1558-5646.1989.tb04226.x (1989).

    Article 
    PubMed 

    Google Scholar 

  • Milligan, B. G. Maximum-likelihood estimation of relatedness. Genetics 163, 1153–1167 (2003).

    PubMed 
    PubMed Central 

    Google Scholar 

  • del Felipe, P. et al. Genetic diversity and structure of the commercially important native fish pacu (Piaractus mesopotamicus) from cultured and wild fish populations: Relevance for broodstock management. Aquacult. Int. 29, 289–305. https://doi.org/10.1007/s10499-020-00626-w (2021).

    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    “Drawing Together” is awarded Norman B. Leventhal City Prize

    Finding community in high-energy-density physics