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Evo-Devo Lessons Learned from Honeybees

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Abstract

Honeybees (Apis mellifera) are hymenopteran insects of importance both economically and scientifically. Honeybees share much of the basic biology of well-studied insect models, such as Drosophila and Tribolium, but their sex determination and embryogenesis differ in important ways, which provide some understanding of the way early-acting developmental pathways evolve. Honeybees also display remarkable polyphenisms, critical to their biology. Understanding how these environmentally induced shifts in developmental trajectory occur is critical to our understanding of the evolution of environmental influences on developmental processes.

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References

  • Amdam GV, Norberg K, Hagen A, Omholt SW (2003a) Social exploitation of vitellogenin. Proc Natl Acad Sci U S A 100(4):1799–1802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amdam GV, Simões ZL, Guidugli KR, Norberg K, Omholt SW (2003b) Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA. BMC Biotechnol 3(1):1

    Article  PubMed  PubMed Central  Google Scholar 

  • Beye M, Hartel S, Hagen A, Hasselmann M, Omholt SW (2002) Specific developmental gene silencing in the honey bee using a homeobox motif. Insect Mol Biol 11(6):527–532

    Article  CAS  PubMed  Google Scholar 

  • Beye M, Hasselmann M, Fondrk MK, Page RE, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114(4):419–429

    Article  CAS  Google Scholar 

  • Buttstedt A, Ihling CH, Pietzsch M, Moritz RF (2016) Royalactin is not a royal making of a queen. Nature 537(7621):E10–E12

    Article  CAS  PubMed  Google Scholar 

  • Cameron R, Duncan E, Dearden P (2013) Biased gene expression in early honeybee larval development. BMC Genomics 14(1):903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cridge A, Lovegrove M, Skelly J, Taylor S, Petersen G, Cameron R, Dearden P (2017) The honeybee as a model insect for developmental genetics. Genesis 55(5):e23019

    Article  Google Scholar 

  • de Azevedo SV, Hartfelder K (2008) The insulin signaling pathway in honey bee (Apis mellifera) caste development—differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J Insect Physiol 54(6):1064–1071

    Article  CAS  PubMed  Google Scholar 

  • Dearden PK (2006) Germ cell development in the honeybee; vasa and nanos expression. BMC Dev Biol 6(6):1–14

    Google Scholar 

  • Dearden PK, Wilson MJ, Sablan L, Osborne PW, Havler M, McNaughton E, Kimura K, Milshina NV, Hasselmann M, Gemp T, Schioett M, Brown SJ, Elsik CG, Holland PW, Kadowaki T, Beye M (2006) Patterns of conservation and change in honey bee developmental genes. Genome Res 16:1376–1384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duncan EJ, Benton MA, Dearden PK (2013) Canonical terminal patterning is an evolutionary novelty. Dev Biol. https://doi.org/10.1016/j.ydbio.2013.02.010

  • Duncan EJ, Johnson TK, Whisstock JC, Warr CG, Dearden PK (2014) Capturing embryonic development from metamorphosis: how did the terminal patterning signalling pathway of Drosophila evolve? Curr Opin Insect Sci 1:45–51

    Article  Google Scholar 

  • Duncan EJ, Hyink O, Dearden PK (2016) Notch signalling mediates reproductive constraint in the adult worker honeybee. Nat Commun 7:12427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elsik CG, Worley KC, Bennett AK, Beye M, Camara F, Childers CP, de Graaf DC, Debyser G, Deng J, Devreese B (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genomics 15(1):86

    Article  PubMed  PubMed Central  Google Scholar 

  • Fleig R (1990) Engrailed expression and body segmentation in the honeybee, Apis mellifera. Rouxs Arch Dev Biol 198:467–473

    Article  CAS  PubMed  Google Scholar 

  • Fleig R, Sander K (1986) Embryogenesis of the honeybee Apis mellifera L. (Hymenoptera: Apidae): an SEM study. Int J Insect Morphol Embryol 15(5):449–462

    Article  Google Scholar 

  • Gallai N, Salles JM, Settele J, Vaissiere BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68(3):810–821

    Article  Google Scholar 

  • Gempe T, Beye M (2011) Function and evolution of sex determination mechanisms, genes and pathways in insects. BioEssays 33(1):52–60. https://doi.org/10.1002/bies.201000043

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gempe T, Hasselmann M, Schiøtt M, Hause G, Otte M, Beye M (2009) Sex determination in honeybees: two separate mechanisms induce and maintain the female pathway. PLoS Biol 7(10):e1000222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X, Su S, Skogerboe G, Dai S, Li W, Li Z, Liu F, Ni R, Guo Y, Chen S (2013) Recipe for a busy bee: microRNAs in honey bee caste determination. PLoS One 8(12):e81661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasselmann M, Gempe T, Schiott M, Nunes-Silva CG, Otte M, Beye M (2008) Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Nature 454(7203):519–522. https://doi.org/10.1038/nature07052

    Article  PubMed  CAS  Google Scholar 

  • Hedges SB, Marin J, Suleski M, Paymer M, Kumar S (2015) Tree of life reveals clock-like speciation and diversification. Mol Biol Evol 32(4):835–845. https://doi.org/10.1093/molbev/msv037

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annu Rev Entomol 53:209–230

    Article  CAS  Google Scholar 

  • Kamakura M (2011) Royalactin induces queen differentiation in honeybees. Nature 473(7348):478–483

    Article  CAS  PubMed  Google Scholar 

  • Kamakura M (2016) Royalactin is not a royal making of a queen Reply. Nature 537(7621):E13–E13

    Article  CAS  PubMed  Google Scholar 

  • Kohno H, Suenami S, Takeuchi H, Sasaki T, Kubo T (2016) Production of knockout mutants by CRISPR/Cas9 in the European honeybee, Apis mellifera L. Zool Sci 33(5):505–512

    Article  CAS  PubMed  Google Scholar 

  • Kritsky G (2017) Beekeeping from antiquity through the middle ages. Annu Rev Entomol 62:249–264

    Article  CAS  PubMed  Google Scholar 

  • Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319(5871):1827–1830

    Article  CAS  PubMed  Google Scholar 

  • Kucharski R, Foret S, Maleszka R (2015) EGFR gene methylation is not involved in Royalactin controlled phenotypic polymorphism in honey bees. Sci Rep 5:14070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C (2006) Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439(7077):728–732

    Article  CAS  PubMed  Google Scholar 

  • Meixner MD, Le Conte Y (2016) A current perspective on honey bee health. Apidologie 47(3):273–275

    Article  Google Scholar 

  • Munoz-Torres MC, Reese JT, Childers CP, Bennett AK, Sundaram JP, Childs KL, Anzola JM, Milshina N, Elsik CG (2010) Hymenoptera genome database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 39(suppl_1):D658–D662

    PubMed  PubMed Central  Google Scholar 

  • Mutti NS, Dolezal AG, Wolschin F, Mutti JS, Gill KS, Amdam GV (2011) IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. J Exp Biol 214(23):3977–3984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson CM, Ihle KE, Fondrk MK, Page RE, Amdam GV (2007) The gene vitellogenin has multiple coordinating effects on social organization. PLoS Biol 5(3):e62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nissen I, Müller M, Beye M (2012) The Am-tra2 gene is an essential regulator of female splice regulation at two levels of the sex determination hierarchy of the honeybee. Genetics 192(3):1015–1026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olesnicky EC, Desplan C (2007) Distinct mechanisms for mRNA localization during embryonic axis specification in the wasp Nasonia. Dev Biol 306(1):134–142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oxley PR, Thompson GJ, Oldroyd BP (2008) Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera). Genetics 179(3):1337–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ronai I, Barton DA, Oldroyd BP, Vergoz V (2015) Regulation of oogenesis in honey bee workers via programed cell death. J Insect Physiol 81:36–41

    Article  CAS  PubMed  Google Scholar 

  • Sander K (1976) Specification of the basic body pattern in insect embryogenesis. Adv Insect Physiol 12:125–238

    Article  Google Scholar 

  • Schulte C, Theilenberg E, Müller-Borg M, Gempe T, Beye M (2014) Highly efficient integration and expression of piggyBac-derived cassettes in the honeybee (Apis mellifera). Proc Natl Acad Sci 111(24):9003–9008

    Article  CAS  PubMed  Google Scholar 

  • Spannhoff A, Kim YK, Raynal NJM, Gharibyan V, Su MB, Zhou YY, Li J, Castellano S, Sbardella G, Issa JPJ (2011) Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep 12(3):238–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tautz J (2008) The buzz about bees: biology of a superorganism. Springer Science & Business Media. Berlin, Heidelberg

    Google Scholar 

  • The Honey Bee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949

    Article  CAS  Google Scholar 

  • Walldorf U, Fleig R, Gehring WJ (1989) Comparison of homeobox-containing genes of the honeybee and Drosophila. Proc Natl Acad Sci U S A 86(24):9971–9975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Jorda M, Jones L, Maleszka R, Ling X, Robertson HM, Mizzen CA, Peinado MA, Robinson GE (2006) Functional CpG methlyation system in a social insect. Science 314:645–647

    Article  CAS  PubMed  Google Scholar 

  • Wilson MJ, Dearden PK (2009) Tailless patterning functions are conserved in the honeybee even in the absence of Torso signaling. Dev Biol 335(1):276–287. https://doi.org/10.1016/j.ydbio.2009.09.002. S0012-1606(09)01174-9 [pii]

    Article  PubMed  CAS  Google Scholar 

  • Wilson MJ, Dearden PK (2011) Diversity in insect axis formation: two orthodenticle genes and hunchback act in anterior patterning and influence dorsoventral organization in the honeybee (Apis mellifera). Development 138(16):3497–3507

    Article  CAS  PubMed  Google Scholar 

  • Wilson MJ, Dearden PK (2012) Pair-rule gene orthologues have unexpected maternal roles in the honeybee (Apis mellifera). PLoS One 7(9):e46490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson MJ, Havler M, Dearden PK (2009) Giant, Kruppel, and caudal act as gap genes with extensive roles in patterning the honeybee embryo. Dev Biol 339(1):200–211

    Article  CAS  PubMed  Google Scholar 

  • Zhu K, Liu M, Fu Z, Zhou Z, Kong Y, Liang H, Lin Z, Luo J, Zheng H, Wan P (2017) Plant microRNAs in larval food regulate honeybee caste development. PLoS Genet 13(8):e1006946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Peter K. Dearden .

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Dearden, P.K. (2018). Evo-Devo Lessons Learned from Honeybees. In: Nuno de la Rosa, L., Müller, G. (eds) Evolutionary Developmental Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-33038-9_178-1

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  • DOI: https://doi.org/10.1007/978-3-319-33038-9_178-1

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  • Print ISBN: 978-3-319-33038-9

  • Online ISBN: 978-3-319-33038-9

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