Dharampal, P. S., Hetherington, M. C. & Steffan, S. A. Microbes make the meal: Oligolectic bees require microbes within their host pollen to thrive. Ecol. Entomol. https://doi.org/10.1111/een.12926 (2020).
Sonnenburg, J. L. & Bäckhed, F. Diet-microbiota interactions as moderators of human metabolism. Nature 535, 56–64 (2016).
Suzuki, T. A. Links between natural variation in the microbiome and host fitness in wild mammals. Integr. Comp. Biol. 57, 756–769 (2017).
Zheng, D., Liwinski, T. & Elinav, E. Interaction between microbiota and immunity in health and disease. Cell Res. 30, 492–506 (2020).
Kwong, W. K., Mancenido, A. L. & Moran, N. A. Immune system stimulation by the native gut microbiota of honey bees. R. Soc. Open Sci. 4, 170003 (2017).
Bo, T.-B. et al. Coprophagy prevention alters microbiome, metabolism, neurochemistry, and cognitive behavior in a small mammal. ISME J. https://doi.org/10.1038/s41396-020-0711-6 (2020).
Sarkar, A. et al. The role of the microbiome in the neurobiology of social behaviour. Biol. Rev. 95, 12603 (2020).
Vernier, C. L. et al. The gut microbiome defines social group membership in honey bee colonies. Sci. Adv. 6, 3431 (2020).
Lemoine, M. M., Engl, T. & Kaltenpoth, M. Microbial symbionts expanding or constraining abiotic niche space in insects. Curr. Opin. Insect Sci. 39, 14–20 (2020).
Engel, P. et al. The bee microbiome: Impact on bee health and model for evolution and ecology of host-microbe interactions. MBio. https://doi.org/10.1128/mBio.02164-15 (2006).
Daisley, B. A., Chmiel, J. A., Pitek, A. P., Thompson, G. J. & Reid, G. Missing microbes in bees: How systematic depletion of key symbionts erodes immunity. Trends Microbiol. https://doi.org/10.1016/j.tim.2020.06.006 (2020).
Bonilla-Rosso, G. & Engel, P. Functional roles and metabolic niches in the honey bee gut microbiota. Curr. Opin. Microbiol. 43, 69–76 (2018).
Zheng, H., Powell, J. E., Steele, M. I., Dietrich, C. & Moran, N. A. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proc. Natl. Acad. Sci. 114, 4775–4780 (2017).
Zheng, H. et al. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. MBio. https://doi.org/10.1128/mBio.01326-16 (2016).
Engel, P. & Moran, N. A. Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes 4, 60–65 (2013).
Lee, F. J., Rusch, D. B., Stewart, F. J., Mattila, H. R. & Newton, I. L. G. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ. Microbiol. 17, 796–815 (2015).
Anderson, K. E. et al. Hive-stored pollen of honey bees: Many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol. Ecol. 23, 5904–5917 (2014).
Dharampal, P. S., Carlson, C., Currie, C. R. & Steffan, S. A. Pollen-borne microbes shape bee fitness. Proc. R. Soc. B Biol. Sci. 286, 20182894 (2019).
Rothman, J. A., Leger, L., Graystock, P., Russell, K. & McFrederick, Q. S. The bumble bee microbiome increases survival of bees exposed to selenate toxicity. Environ. Microbiol. 21, 1462–2920. https://doi.org/10.1111/1462-2920.14641 (2019).
Wu, Y. et al. Honey bee ( Apis mellifera ) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract. Microb. Biotechnol. 13, 1201–1212 (2020).
Praet, J. et al. Large-scale cultivation of the bumblebee gut microbiota reveals an underestimated bacterial species diversity capable of pathogen inhibition. Environ. Microbiol. 20, 214–227 (2018).
Forsgren, E., Olofsson, T. C., Vásquez, A. & Fries, I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41, 99–108 (2010).
Cariveau, D. P., Elijah Powell, J., Koch, H., Winfree, R. & Moran, N. A. Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J. 8, 2369–2379 (2014).
Raymann, K., Shaffer, Z. & Moran, N. A. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol. 15, e2001861 (2017).
Schwarz, R. S., Moran, N. A. & Evans, J. D. Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proc. Natl. Acad. Sci. 113, 9345–9350 (2016).
Maes, P. W., Rodrigues, A. P., Oliver, R., Mott, B. M. & Anderson, K. E. Diet related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honey bee (Apis mellifera). Mol. Ecol. 25, 5439–5450 (2016).
Koch, H. & Schmid-Hempel, P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl. Acad. Sci. 108, 19288–19292 (2011).
Evans, J. D. & Lopez, D. L. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 97, 752–756 (2004).
Emery, O., Schmidt, K. & Engel, P. Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Mol. Ecol. 26, 2576–2590 (2017).
Engel, P., Martinson, V. G. & Moran, N. A. Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. 109, 11002–11007 (2012).
Kwong, W. K. & Moran, N. A. Gut microbial communities of social bees. Nat. Rev. Micro 14, 374–384 (2016).
McFrederick, Q. S. & Rehan, S. M. Characterization of pollen and bacterial community composition in brood provisions of a small carpenter bee. Mol. Ecol. 25, 2302–2311 (2016).
McFrederick, Q. S. et al. Flowers and wild megachilid bees share microbes. Microb. Ecol. 73, 188–200 (2017).
McFrederick, Q. S. et al. Environment or kin: whence do bees obtain acidophilic bacteria?. Mol. Ecol. 21, 1754–1768 (2012).
McFrederick, Q. S., Wcislo, W. T., Hout, M. C. & Mueller, U. G. Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees. FEMS Microbiol. Ecol. 88, 398–406 (2014).
Graystock, P., Rehan, S. M. & McFrederick, Q. S. Hunting for healthy microbiomes: Determining the core microbiomes of Ceratina, Megalopta, and Apis bees and how they associate with microbes in bee collected pollen. Conserv. Genet. 18, 701–711 (2017).
McFrederick, Q. S. et al. Specificity between lactobacilli and hymenopteran hosts is the exception rather than the rule. Appl. Environ. Microbiol. 79, 1803–1812 (2013).
Sanders, J. G. et al. Stability and phylogenetic correlation in gut microbiota: Lessons from ants and apes. Mol. Ecol. 23, 1268–1283 (2014).
Kwong, W. K. et al. Dynamic microbiome evolution in social bees. Sci. Adv. 3, 1–17 (2017).
Rothman, J. A., Andrikopoulos, C., Cox-Foster, D. & McFrederick, Q. S. Floral and foliar source affect the bee nest microbial community. Microb. Ecol. 78, 506–516 (2019).
Cohen, H., McFrederick, Q. S. & Philpott, S. M. Environment shapes the microbiome of the blue orchard bee, Osmia lignaria. Microb. Ecol. 80, 897–907 (2020).
Muñoz-Colmenero, M. et al. Differences in honey bee bacterial diversity and composition in agricultural and pristine environments—A field study. Apidologie. https://doi.org/10.1007/s13592-020-00779-w (2020).
Kapheim, K. M. et al. Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS ONE 10, 1–14 (2015).
Elijah Powell, J., Eiri, D., Moran, N. A. & Rangel, J. Modulation of the honey bee queen microbiota: Effects of early social contact. PLoS ONE 13, 1–14 (2018).
Tarpy, D. R., Mattila, H. R. & Newton, I. L. G. Development of the honey bee gut microbiome throughout the queen-rearing process. Appl. Environ. Microbiol. 81, 3182–3191 (2015).
Dong, Z. X. et al. Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiol. Res. 231, 126370 (2020).
D’Alvise, P. et al. The impact of winter feed type on intestinal microbiota and parasites in honey bees. Apidologie 49, 252–264 (2018).
Huang, S. K. et al. Influence of feeding type and Nosema ceranae infection on the gut microbiota of Apis cerana workers. mSystems 3, 177–195 (2018).
Rothman, J. A., Carroll, M. J., Meikle, W. G., Anderson, K. E. & McFrederick, Q. S. Longitudinal effects of supplemental forage on the Honey Bee (Apis mellifera) microbiota and inter- and intra-colony variability. Microb. Ecol. 76, 814–824 (2018).
Zhang, Y. et al. Nosema ceranae infection enhances Bifidobacterium spp. abundances in the honey bee hindgut. Apidologie 50, 353–362 (2019).
Danforth, B. N., Minckley, R. L. & Neff, J. L. The Solitary Bees (Princeton University Press, Princeton, 2019).
Santos, P. K. F., Arias, M. C. & Kapheim, K. M. Loss of developmental diapause as prerequisite for social evolution in bees. Biol. Lett. 15, 20190398 (2019).
Harmon-Threatt, A. Influence of nesting characteristics on health of wild bee communities. Annu. Rev. Entomol. 65, 39–56 (2020).
Johansen, C., Mayer, D., Stanford, A. & Kious, C. Alkali Bees: Their Biology and Management for Alfalfa Seed Production in the Pacific Northwest (Publication, Pacific Northwest Cooperative Extension Service, Genesee, 1982).
Cane, J. H. A native ground-nesting bee (Nomia melanderi) sustainably managed to pollinate alfalfa across an intensively agricultural landscape. Apidologie 39, 315–323 (2008).
Cane, J. H. Pollinating bees (Hymenoptera: Apiformes) of U.S. alfalfa compared for rates of pod and seed set. J. Econ. Entomol. 95, 22–27 (2002).
Batra, S. W. & Bohart, G. E. Alkali bees: Response of adults to pathogenic fungi in brood cells. Science 165, 607 (1969).
Galbraith, D. A. et al. Investigating the viral ecology of global bee communities with high-throughput metagenomics. Sci. Rep. 8, 1–11 (2018).
Bohart, G. E., Stephen, W. P. & Eppley, E. K. The biology of Heterostylum robustum (Diptera: Bombyliidae), a parasite of the alkali bee. Ann. Entomol. Soc. Am. 53, 425–435 (1960).
Johansen, C. A., Mayer, D. F. & Eves, J. D. Biology and management of the alkali bee, Nomia melanderi Cockrell (Hymenoptera: Halictidae).Melanderii Cockrell (Hymenoptera: Halictidae).Melanderi (Washington State Entomology, Pullman, 1978).
Johansen, C. A. & Mayer, D. F. Pollinator Protection: A Bee and Pesticide Handbook (Wicwas Press, Kalamazoo, 1990).
Stephen, W. P. Solitary bees in North American agriculture: A perspective. In For Nonnative Crops, Whence Pollinators of the Future? (eds Strickler, K. & Cane, J. H.) 41–66 (Entomological Society of America, Annapolis, 2003).
Kapheim, K. M. et al. Draft genome assembly and population genetics of an agricultural pollinator, the solitary alkali bee (Halictidae: Nomia melanderi). G3 9, 625–634 (2019).
Batra, S. W. T. Aggression, territoriality, mating and nest aggregation of some solitary bees (Hymenoptera: Halictidae, Megachilidae, Colletidae, Anthophoridae). J. Kansas Entomol. Soc. 51, 547–559 (1978).
Mayer, D. F. & Miliczky, E. R. Emergence, male behavior, and mating in the alkali bee, Nomia melanderi Cockerell (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 71, 61–68 (1998).
Kapheim, K. M. & Johnson, M. M. Juvenile hormone, but not nutrition or social cues, affects reproductive maturation in solitary alkali bees (Nomia melanderi). J. Exp. Biol. https://doi.org/10.1242/jeb.162255 (2017).
Koch, H. & Schmid-Hempel, P. Bacterial communities in central European bumble bees: Low diversity and high specificity. Microb. Ecol. 62, 121–133 (2011).
Martinson, V. G., Moy, J. & Moran, N. A. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl. Environ. Microbiol. 78, 2830–2840 (2012).
Powell, J. E., Martinson, V. G., Urban-Mead, K. & Moran, N. A. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl. Environ. Microbiol. 80, 7378–7387 (2014).
Kapheim, K. M. & Johnson, M. M. Support for the reproductive ground plan hypothesis in a solitary bee: Links between sucrose response and reproductive status. Proc. R. Soc. B Biol. Sci. 284, 20162406 (2017).
R Core Team. R: A Language and Environment for Statistical Computing (2019).
McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217 (2013).
Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. BioRxiv. https://doi.org/10.1101/221499 (2017).
Jari Oksanen, F. et al. vegan: Community Ecology Package (2019).
McMurdie, P. J. & Holmes, S. Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol. 10, e1003531 (2014).
Anderson, M. J., Ellingsen, K. E. & McArdle, B. H. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9, 683–693 (2006).
Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Lenth, R. emmeans: Estimated Marginal Means, Aka Least-Squares Means (2020).
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
Lahti, L. & Shetty, S. Microbiome R Package (2012).
Zheng, J. et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int. J. Syst. Evol. Microbiol. 70, 2782–2858 (2020).
Rummel, P. S. et al. Maize root and shoot litter quality controls short-term emissions and bacterial community structure of arable soil. Biogeosciences 17, 1181–1198 (2020).
McFrederick, Q. S., Vuong, H. Q. & Rothman, J. A. Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers. Int. J. Syst. Evol. Microbiol. 68, 1879–1884 (2018).
Wittouck, S., Wuyts, S., Meehan, C. J., van Noort, V. & Lebeer, S. A genome-based species taxonomy of the Lactobacillus genus complex. mSystems. https://doi.org/10.1128/mSystems.00264-19 (2019).
Engel, P. & Moran, N. A. The gut microbiota of insects—Diversity in structure and function. FEMS Microbiol. Rev. 37, 699–735 (2013).
Cane, J. H., Dobson, H. E. M. & Boyer, B. Timing and size of daily pollen meals eaten by adult females of a solitary bee (Nomia melanderi) (Apiformes: Halictidae). Apidologie 48, 17–30 (2016).
Engel, P., Bartlett, K. D. & Moran, N. A. The bacterium Frischella perrara causes scab formation in the gut of its honeybee host. MBio 6, 1–8 (2015).
Martinson, V. G. et al. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20, 619–628 (2011).
Vásquez, A. & Olofsson, T. C. The lactic acid bacteria involved in the production of bee pollen and bee bread. J. Apic. Res. 48, 189–195 (2009).
Vuong, H. Q. & McFrederick, Q. S. Comparative genomics of wild bee and flower isolated Lactobacillus reveals potential adaptation to the bee host. Genome Biol. Evol. 11, 2151–2161 (2019).
Source: Ecology - nature.com
