in

Bumble bees exhibit body size clines across an urban gradient despite low genetic differentiation

[adace-ad id="91168"]
  • Corlett, R. T. The Anthropocene concept in ecology and conservation. Trends Ecol. Evol. 30, 36–41 (2015).

    PubMed 

    Google Scholar 

  • IPBES. Summary for Policymakers of the Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES Secretariat, 2019).

    Google Scholar 

  • Vitousek, P. M. Human domination of Earth’s ecosystems. Science 277, 494–499 (1997).

    CAS 

    Google Scholar 

  • Wong, B. B. M. & Candolin, U. Behavioral responses to changing environments. Behav. Ecol. 26, 665–673 (2015).

    Google Scholar 

  • Hale, R. & Swearer, S. E. Ecological traps: Current evidence and future directions. Proc. R. Soc. B Biol. Sci. 283, 1–8 (2016).

    Google Scholar 

  • Charman, T. G., Sears, J., Green, R. E. & Bourke, A. F. G. Conservation genetics, foraging distance and nest density of the scarce Great Yellow Bumblebee (Bombus distinguendus). Mol. Ecol. 19, 2661–2674 (2010).

    PubMed 

    Google Scholar 

  • Violle, C. et al. Let the concept of trait be functional!. Oikos 116, 882–892 (2007).

    Google Scholar 

  • Husemann, M., Zachos, F. E., Paxton, R. J. & Habel, J. C. Effective population size in ecology and evolution. Heredity 117, 191–192 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wagner, D. L. Insect declines in the Anthropocene. Annu. Rev. Entomol. 65, 457–480 (2020).

    CAS 
    PubMed 

    Google Scholar 

  • Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).

    PubMed 

    Google Scholar 

  • Thogmartin, W. E. et al. Monarch butterfly population decline in North America: Identifying the threatening processes. R. Soc. Open Sci. 4, 170760 (2017).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. U.S.A. 108, 662–667 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Burkle, L. A., Marlin, J. C. & Knight, T. M. Plant-pollinator interactions over 120 years: Loss of species, co-occurrence, and function. Science 340, 1611–1615 (2013).

    ADS 

    Google Scholar 

  • Grixti, J. C., Wong, L. T., Cameron, S. A. & Favret, C. Decline of bumble bees (Bombus) in the North American Midwest. Biol. Conserv. 142, 75–84 (2009).

    Google Scholar 

  • Goulson, D. Bumblebees: Behaviour, Ecology, and Conservation (Oxford University Press, Oxford, 2010).

    Google Scholar 

  • Colla, S. R., Gadallah, F., Richardson, L., Wagner, D. & Gall, L. Assessing declines of North American bumble bees (Bombus spp.) using museum specimens. Biodivers. Conserv. 21, 3585–3595 (2012).

    Google Scholar 

  • Hatfield, R. et al. IUCN assessments of North American Bombus spp. http://www.xerces.org/ (2015).

  • Arbetman, M. P., Gleiser, G., Morales, C. L., Williams, P. & Aizen, M. A. Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence. Proc. R. Soc. B Biol. Sci. 284, 20170204 (2017).

    Google Scholar 

  • Bommarco, R. et al. Dispersal capacity and diet breadth modify the response of wild bees to habitat loss. Proc. R. Soc. B Biol. Sci. 277, 2075–2082 (2010).

    Google Scholar 

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

    PubMed 

    Google Scholar 

  • Banaszak-Cibicka, W. & Żmihorski, M. Wild bees along an urban gradient: Winners and losers. J. Insect Conserv. 16, 331–343 (2012).

    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 

  • Thompson, M.J., Capilla-Lasheras, P.C., Dominoni, D.M., Réale, D. & Charmantier, A. Phenotypic variation in urban environments: mechanisms and implications. Trends Ecol. Evol. 37, 171–182 (2022).

    CAS 
    PubMed 

    Google Scholar 

  • Peat, J., Tucker, J. & Goulson, D. Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers?. Ecol. Entomol. 30, 176–181 (2005).

    Google Scholar 

  • Greenleaf, S. S., Williams, N. M., Winfree, R. & Kremen, C. Bee foraging ranges and their relationship to body size. Oecologia 153, 589–596 (2007).

    ADS 
    PubMed 

    Google Scholar 

  • Spaethe, J. & Weidenmüller, A. Size variation and foraging rate in bumblebees (Bombus terrestris). Insectes Soc. 49, 142–146 (2002).

    Google Scholar 

  • Couvillon, M. J. & Dornhaus, A. Small worker bumble bees (Bombus impatiens) are hardier against starvation than their larger sisters. Insectes Soc. 57, 193–197 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pendrel, B. A. & Plowright, R. C. Larval feeding by adult bumble bee workers (Hymenoptera: Apidae). Behav. Ecol. Sociobiol. 8, 71–76 (1981).

    Google Scholar 

  • Sutcliffe, G. H. & Plowright, R. C. The effects of food supply on adult size in the bumble bee Bombus terricola Kirby (Hymenoptera: Apidae). Can. Entomol. 120, 1051–1058 (1988).

    Google Scholar 

  • Couvillon, M. J. & Dornhaus, A. Location, location, location: Larvae position inside the nest is correlated with adult body size in worker bumble-bees (Bombus impatiens). Proc. R. Soc. B Biol. Sci. 276, 2411–2418 (2009).

    Google Scholar 

  • Bartomeus, I. et al. Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc. Natl. Acad. Sci. U.S.A. 110, 4656–4660 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Austin, M. W. & Dunlap, A. S. Intraspecific variation in worker body size makes North American bumble bees (Bombus spp.) less susceptible to decline. Am. Nat. 194, 381–394 (2019).

    PubMed 

    Google Scholar 

  • Watters, J. V., Lema, S. C. & Nevitt, G. A. Phenotype management: A new approach to habitat restoration. Biol. Conserv. 112, 435–445 (2003).

    Google Scholar 

  • Haddaway, N. R., Mortimer, R. J. G., Christmas, M., Grahame, J. W. & Dunn, A. M. Morphological diversity and phenotypic plasticity in the threatened British white-clawed crayfish (Austropotamobius pallipes). Aquat. Conserv. Mar. Freshw. Ecosyst. 22, 220–231 (2012).

    Google Scholar 

  • Lema, S. C. & Nevitt, G. A. Testing an ecophysiological mechanism of morphological plasticity in pupfish and its relevance to conservation efforts for endangered Devils Hole pupfish. J. Exp. Biol. 209, 3499–3509 (2006).

    PubMed 

    Google Scholar 

  • Crispo, E. Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J. Evol. Biol. 21, 1460–1469 (2008).

    CAS 
    PubMed 

    Google Scholar 

  • Fraser, D. J. & Bernatchez, L. Adaptive evolutionary conservation: Towards a unified concept for defining conservation units. Mol. Ecol. 10, 2741–2752 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684–692 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Spielman, D., Brook, B. W. & Frankham, R. Most species are not driven to extinction before genetic factors impact them. Proc. Natl. Acad. Sci. U.S.A. 101, 15261–15264 (2004).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Woodard, S. H. et al. Molecular tools and bumble bees: Revealing hidden details of ecology and evolution in a model system. Mol. Ecol. 24, 2916–2936 (2015).

    MathSciNet 
    PubMed 

    Google Scholar 

  • Lozier, J. D., Strange, J. P., Stewart, I. J. & Cameron, S. A. Patterns of range-wide genetic variation in six North American bumble bee (Apidae: Bombus) species. Mol. Ecol. 20, 4870–4888 (2011).

    PubMed 

    Google Scholar 

  • Williams, B. L., Brawn, J. D. & Paige, K. N. Landscape scale genetic effects of habitat fragmentation on a high gene flow species: Speyeria idalia (Nymphalidae). Mol. Ecol. 12, 11–20 (2003).

    CAS 
    PubMed 

    Google Scholar 

  • IUCN. The IUCN Red List of Threatened Species. https://www.iucnredlist.org. Accessed 18 Dec 2019 (2019).

  • MacPhail, V. J., Richardson, L. L. & Colla, S. R. Incorporating citizen science, museum specimens, and field work into the assessment of extinction risk of the American Bumble bee (Bombus pensylvanicus De Geer 1773) in Canada. J. Insect Conserv. 23, 597–611 (2019).

    Google Scholar 

  • Camilo, G. R., Muñiz, P. A., Arduser, M. S. & Spevak, E. M. A checklist of the bees (Hymenoptera: Apoidea) of St. Louis, Missouri, USA. J. Kansas Entomol. Soc. 90, 175–188 (2018).

    Google Scholar 

  • United States Census Bureau. Land Area and Persons Per Square Mile. https://www.census.gov/quickfacts/fact/note/US/LND110210. Accessed 26 March 2020 (2010).

  • United States Census Bureau. City and Town Population Totals: 2010–2018. https://www.census.gov/data/tables/time-series/demo/popest/2010s-total-cities-and-towns.html. Accessed 26 March 2020 (2020).

  • Thompson, K. & Jones, A. Human population density and prediction of local plant extinction in Britain. Conserv. Biol. 13, 185–189 (1999).

    Google Scholar 

  • Fontana, C. S., Burger, M. I. & Magnusson, W. E. Bird diversity in a subtropical South-American City: Effects of noise levels, arborisation and human population density. Urban Ecosyst. 14, 341–360 (2011).

    Google Scholar 

  • Lepais, O. et al. Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol. Ecol. 19, 819–831 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Holehouse, K. A., Hammond, R. L. & Bourke, A. F. G. Non-lethal sampling of DNA from bumble bees for conservation genetics. Insectes Soc. 50, 277–285 (2003).

    Google Scholar 

  • Williams, P. H., Thorp, R., Richardson, L. & Colla, S. R. Bumble Bees of North America (Princeton University Press, 2014).

    Google Scholar 

  • Cane, J. H. Estimation of bee size using intertegular span (Apoidea). J. Kansas Entomol. Soc. 60, 145–147 (1987).

    Google Scholar 

  • Walsh, P. S., Metzger, D. A. & Higuchi, R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513 (1991).

    CAS 
    PubMed 

    Google Scholar 

  • 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 

  • 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 

  • Funk, C. R., Schmid-Hempel, R. & Schmid-Hempel, P. Microsatellite loci for Bombus spp. Mol. Ecol. Notes 6, 83–86 (2006).

    CAS 

    Google Scholar 

  • Stolle, E. et al. Novel microsatellite DNA loci for Bombus terrestris (Linnaeus, 1758). Mol. Ecol. Resour. 9, 1345–1352 (2009).

    CAS 
    PubMed 

    Google Scholar 

  • Kearse, M. et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649 (2012).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Chapman, R. E. & Bourke, A. F. G. The influence of sociality on the conservation biology of social insects. Ecol. Lett. 4, 650–662 (2001).

    Google Scholar 

  • Geib, J. C., Strange, J. P. & Galen, A. Bumble bee nest abundance, foraging distance, and host-plant reproduction: Implications for management and conservation. Ecol. Appl. 25, 768–778 (2015).

    PubMed 

    Google Scholar 

  • Chakraborty, R., Andrade, M. D. E., Daiger, S. P. & Budowle, B. Apparent heterozygote deficiencies observed in DNA typing data and their implications in forensic applications. Ann. Hum. Genet. 56, 45–57 (1992).

    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Gruber, B. & Adamack, A. T. PopGenReport: Simplifying basic population genetic analyses in R. Methods Ecol. Evol. 5, 384–387 (2014).

    Google Scholar 

  • Wang, J. Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963–1979 (2004).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Crozier, R. H. Genetics of sociality. In Social Insects Vol. I (ed. Hermann, H. R.) 223–286 (Academic Press, 1979).

    Google Scholar 

  • 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 

  • Leberg, P. L. Estimating allelic richness: Effects of sample size and bottlenecks. Mol. Ecol. 11, 2445–2449 (2002).

    CAS 
    PubMed 

    Google Scholar 

  • Goudet, J. hierfstat, a package for r to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186 (2005).

    Google Scholar 

  • Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).

    CAS 

    Google Scholar 

  • Ryman, N. & Palm, S. POWSIM: A computer program for assessing statistical power when testing for genetic differentiation. Mol. Ecol. Notes 6, 600–602 (2006).

    Google Scholar 

  • Zayed, A. & Packer, L. High levels of diploid male production in a primitively eusocial bee (Hymenoptera: Halictidae). Heredity 87, 631–636 (2001).

    CAS 
    PubMed 

    Google Scholar 

  • 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 

  • Hale, M. L., Burg, T. M. & Steeves, T. E. Sampling for microsatellite-based population genetic studies: 25 to 30 Individuals per population is enough to accurately estimate allele frequencies. PLoS One 7, e45170 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lenth, R. V. Least-squares means: The R package lsmeans. J. Stat. Softw. 69, 1–33 (2016).

    Google Scholar 

  • Fitzpatrick, S. W. et al. Gene flow constrains and facilitates genetically based divergence in quantitative traits. Copeia 105, 462–474 (2017).

    Google Scholar 

  • Price, T. D., Qvarnström, A. & Irwin, D. E. The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. B Biol. Sci. 270, 1433–1440 (2003).

    Google Scholar 

  • Liu, B.-J., Zhang, B.-D., Xue, D.-X., Gao, T.-X. & Liu, J.-X. Population structure and adaptive divergence in a high gene flow marine fish: The small yellow croaker (Larimichthys polyactis). PLoS One 11, e0154020 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Vaudo, A. D., Tooker, J. F., Grozinger, C. M. & Patch, H. M. Bee nutrition and floral resource restoration. Curr. Opin. Insect Sci. 10, 133–141 (2015).

    PubMed 

    Google Scholar 

  • Woodard, S. H. & Jha, S. Wild bee nutritional ecology: Predicting pollinator population dynamics, movement, and services from floral resources. Curr. Opin. Insect Sci. 21, 83–90 (2017).

    PubMed 

    Google Scholar 

  • Keller, L. F. & Waller, D. M. Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241 (2002).

    Google Scholar 

  • Sivakoff, F. S. & Gardiner, M. M. Soil lead contamination decreases bee visit duration at sunflowers. Urban Ecosyst. 20, 1221–1228 (2017).

    Google Scholar 

  • Whitehorn, P. R., Norville, G., Gilburn, A. & Goulson, D. Larval exposure to neonicotinoid imidacloprid impacts adult size in the farmland butterfly Pieris brassicae. PeerJ 6, e4772 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Merckx, T., Kaiser, A. & Van Dyck, H. Increased body size along urbanization gradients at both community and intraspecific level in macro-moths. Glob. Change Biol. 24, 3837–3848 (2018).

    ADS 

    Google Scholar 

  • Oliveira, M. O., Brito, T. F., Campbell, A. J. & Contrera, F. A. L. Body size and corbiculae area variation of the stingless bee Melipona fasciculata Smith, 1854 (Apidae, Meliponini) under different levels of habitat quality in the eastern Amazon. Entomol. Gen. 39, 45–52 (2019).

    Google Scholar 

  • Warzecha, D., Diekötter, T., Wolters, V. & Jauker, F. Intraspecific body size increases with habitat fragmentation in wild bee pollinators. Landsc. Ecol. 31, 1449–1455 (2016).

    Google Scholar 

  • Theodorou, P., Baltz, L. M., Paxton, R. J. & Soro, A. Urbanization is associated with shifts in bumblebee body size, with cascading effects on pollination. Evol. Appl. 14, 53–68 (2021).

    PubMed 

    Google Scholar 

  • Strange, J. P. & Tripodi, A. D. Characterizing bumble bee (Bombus) communities in the United States and assessing a conservation monitoring method. Ecol. Evol. 9, 1061–1069 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 


  • Source: Ecology - nature.com

    MIT ReACT welcomes first Afghan cohort to its largest-yet certificate program

    Using nature’s structures in wooden buildings