Gene co-citation networks associated with worker sterility in honey bees

BMC Systems Biology

Graham James Thompson¹  Alanna Gabrielle Backx²  Mark Daley¹  Emma Kate Mullen¹ 

[1] The University of Western Ontario, 1151 Richmond Street North, London, ON N6A 5B7, Canada;Ontario Veterinary College, University of Guelph, 411 Gordon Street, Guelph, Ontario N1G 2W1, Canada

关键词: Pheromone;    Ovaries;    Reproductive altruism;    Hub gene;    Gene expression;    Co-citation network;    Apis mellifera;   

Others  :  866608
DOI  :  10.1186/1752-0509-8-38

 received in 2014-01-23, accepted in 2014-03-18,  发布年份 2014

【 摘 要 】

Background

The evolution of reproductive self-sacrifice is well understood from kin theory, yet our understanding of how actual genes influence the expression of reproductive altruism is only beginning to take shape. As a model in the molecular study of social behaviour, the honey bee Apis mellifera has yielded hundreds of genes associated in their expression with differences in reproductive status of females, including genes directly associated with sterility, yet there has not been an attempt to link these candidates into functional networks that explain how workers regulate sterility in the presence of queen pheromone. In this study we use available microarray data and a co-citation analysis to describe what gene interactions might regulate a worker’s response to ovary suppressing queen pheromone.

Results

We reconstructed a total of nine gene networks that vary in size and gene composition, but that are significantly enriched for genes of reproductive function. The networks identify, for the first time, which candidate microarray genes are of functional importance, as evidenced by their degree of connectivity to other genes within each of the inferred networks. Our study identifies single genes of interest related to oogenesis, including eggless, and further implicates pathways related to insulin, ecdysteroid, and dopamine signaling as potentially important to reproductive decision making in honey bees.

Conclusions

The networks derived here appear to be variable in gene composition, hub gene identity, and the overall interactions they describe. One interpretation is that workers use different networks to control personal reproduction via ovary activation, perhaps as a function of age or environmental circumstance. Alternatively, the multiple networks inferred here may represent segments of the larger, single network that remains unknown in its entirety. The networks generated here are provisional but do offer a new multi-gene framework for understanding how honey bees regulate personal reproduction within their highly social breeding system.

【 授权许可】

   
2014 Mullen et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Hamilton WD: The genetical evolution of social behaviour, I and II. J Theoret Biol 1964, 7:1-52.
• [2]Bourke AFG: Principles of social evolution. Oxford: Oxford University Press; 2011.
• [3]Lehmann L, Keller L: The evolution of cooperation and altruism - a general framework and a classification of models. J Evol Biol 2006, 19:1365-1376.
• [4]Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, Maleszka R, Robertson HM, Weaver DB: Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443:931-949.
• [5]Gadau J, Helmkampf M, Nygaard S, Roux J, Simola DF, Smith CR, Suen G, Wurm Y, Smith CD: The genomic impact of 100 million years of social evolution in seven ant species. Trends Genet 2012, 28:14-21.
• [6]Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M: The genome of the social amoeba Dictyostelium discoideum. Nature 2005, 435:43-57.
• [7]Amdam GV, Norberg K, Fondrk MK, Page RE: Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc Natl Acad Sci U S A 2004, 101:11350-11355.
• [8]Thompson GJ, Kucharski R, Maleszka R, Oldroyd BP: Genome-wide analysis of genes related to ovary activation in worker honey bees. Insect Mol Biol 2008, 17:657-665.
• [9]Thompson GJ, Kucharski R, Maleszka R, Oldroyd BP: Towards a molecular definition of worker sterility: differential gene expression and reproductive plasticity in honey bees. Insect Mol Biol 2006, 15:637-644.
• [10]Grozinger CM, Fan YL, Hoover SER, Winston ML: Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Mol Ecol 2007, 16:4837-4848.
• [11]Cardoen D, Wenseleers T, Ernst UR, Danneels EL, Laget D, De Graaf DC, Schoofs L, Verleyen P: Genome-wide analysis of alternative reproductive phenotypes in honeybee workers. Mol Ecol 2011, 20:4070-4084.
• [12]Wang Y, Kocher SD, Linksvayer TA, Grozinger CM, Page RE, Amdam GV: Regulation of behaviorally associated gene networks in worker honey bee ovaries. J Exp Biol 2012, 215:124-134.
• [13]Paul RK, Takeuchi H, Kubo T: Expression of two ecdysteroid-regulated genes, broad-complex and E75, in the brain and ovary of the honeybee (Apis mellifera L.). Zool Sci 2006, 23:1085-1092.
• [14]Robinson GE, Fernald RD, Clayton DF: Genes and social behavior. Science 2008, 322:896-900.
• [15]Sumner S: Determining the molecular basis of sociality in insects: progress, prospects and potential in sociogenomics. Ann Zool Fenn 2006, 43:423-442.
• [16]Seeley TD: Honeybee ecology: a study of adaptation in social life. Princeton University Press: Princeton; 1985.
• [17]Velthuis HH: Ovarian development in Apis mellifera worker bees. Entomol Exp Appl 1970, 13:377-394.
• [18]Backx AG, Guzman-Novoa E, Thompson GJ: Factors affecting ovary activation in honey bee workers: a meta-analysis. Insect Soc 2012, 59:381-388.
• [19]Barron AB, Robinson GE: The utility of behavioral models and modules in molecular analyses of social behavior. Genes Brain Behav 2008, 7:257-265.
• [20]Hoover SER, Keeling CI, Winston ML, Slessor KN: The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 2003, 90:477-480.
• [21]Le Conte Y, Hefetz A: Primer pheromones in social hymenoptera. Annu Rev Entomol 2008, 53:523-542.
• [22]Visscher PK: A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 1989, 25:247-254.
• [23]Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE: Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci U S A 2003, 100:14519-14525.
• [24]Kocher SD, Ayroles JF, Stone EA, Grozinger CM: Individual variation in pheromone response correlates with reproductive traits and brain gene expression in worker honey bees. Plos One 2010, 5(2):e9116.
• [25]Alaux C, Le Conte Y, Adams HA, Rodriguez-Zas S, Grozinger CM, Sinha S, Robinson GE: Regulation of brain gene expression in honey bees by brood pheromone. Genes Brain Behav 2009, 8:309-319.
• [26]Bloch G, Grozinger CM: Social molecular pathways and the evolution of bee societies. Phil T R Soc B 2011, 366:2155-2170.
• [27]Barabasi AL, Oltvai ZN: Network biology: understanding the cell's functional organization. Nat Rev Genet 2004, 5:101-113.
• [28]Jensen LJ, Saric J, Bork P: Literature mining for the biologist: from information retrieval to biological discovery. Nat Rev Genet 2006, 7:119-129.
• [29]Newman MEJ: Networks : an introduction. Oxford: Oxford University Press; 2010.
• [30]Jeong H, Mason SP, Barabasi AL, Oltvai ZN: Lethality and centrality in protein networks. Nature 2001, 411:41-42.
• [31]Drapeau MD, Albert S, Kucharski R, Prusko C, Maleszka R: Evolution of the yellow/major royal jelly protein family and the emergence of social behavior in honey bees. Genome Res 2006, 16:1385-1394.
• [32]Wheeler DE, Buck N, Evans JD: Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol Biol 2006, 15:597-602.
• [33]Cristino AS, Nunes FMF, Lobo CH, Bitondi MMG, Simoes ZLP, Costa LD, Lattorff HMG, Moritz RFA, Evans JD, Hartfelder K: Caste development and reproduction: a genome-wide analysis of hallmarks of insect eusociality. Insect Mol Biol 2006, 15:703-714.
• [34]Hunt GJ, Amdam GV, Schlipalius D, Emore C, Sardesai N, Williams CE, Rueppell O, Guzman-Novoa E, Arechavaleta-Velasco M, Chandra S, Fondrk MK, Beye M, Page RE: Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 2007, 94:247-267.
• [35]Amdam GV, Csondes A, Fondrk MK, Page RE: Complex social behaviour derived from maternal reproductive traits. Nature 2006, 439:76-78.
• [36]Wang Y, Kaftanoglu O, Siegel AJ, Page RE, Amdam GV: Surgically increased ovarian mass in the honey bee confirms link between reproductive physiology and worker behavior. J Insect Physiol 2010, 56:1816-1824.
• [37]Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M, Andre JB, van Baalen M, Balloux F, Balshine S: Inclusive fitness theory and eusociality. Nature 2011, 471:E1-E4.
• [38]Toth AL, Varala K, Newman TC, Miguez FE, Hutchison SK, Willoughby DA, Simons JF, Egholm M, Hunt JH, Hudson ME, Robinson GE: Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 2007, 318:441-444.
• [39]Plettner E, Slessor KN, Winston ML, Robinson GE, Page RE: Mandibular gland components and ovarian development as measures of caste differentiation in the honey-bee (Apis-Mellifera L). J Insect Physiol 1993, 39:235-240.
• [40]Whitfield CW, Band MR, Bonaldo MF, Kumar CG, Liu L, Pardinas JR, Robertson HM, Soares MB, Robinson GE: Annotated expressed sequence tags and cDNA microarrays for studies of brain and behavior in the honey bee. Genome Res 2002, 12:555-566.
• [41]Munoz-Torres MC, Reese JT, Childers CP, Bennett AK, Sundaram JP, Childs KL, Anzola JM, Milshina N, Elsik CG: Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res 2011, 39:D658-D662.
• [42]Jasny BR, Bloom FE: Flying to new heights. Science 2000, 287:2157-2157.
• [43]Frisch M, Klocke B, Haltmeier M, Frech K: LitInspector: literature and signal transduction pathway mining in PubMed abstracts. Nucleic Acids Res 2009, 37:W135-W140.
• [44]Bairoch A, Bougueleret L, Altairac S, Amendolia V, Auchincloss A, Puy GA: The universal protein resource (UniProt). Nucleic Acids Res 2007, 35:D193-D197.
• [45]Berriz GF, King OD, Bryant B, Sander C, Roth FP: Characterizing gene sets with FuncAssociate. Bioinformatics 2003, 19:2502-2504.
• [46]Backx AG: Genetic components to worker sterility in the honey bee. London: The University of Western Ontario; 2011.
• [47]Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M, Thompson GJ, Zou Z, Hultmark D: Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 2006, 15:645-656.
• [48]Wilson MJ, Abbott H, Dearden PK: The evolution of oocyte patterning in insects: multiple cell-signaling pathways are active during honeybee oogenesis and are likely to play a role in axis patterning. Evol Dev 2011, 13:127-137.
• [49]Warrior R: Primordial germ-cell migration and the assembly of the Drosophila embryonic gonad. Dev Biol 1994, 166:180-194.
• [50]Grigorov MG: Global properties of biological networks. Drug Discov Today 2005, 10:365-372.
• [51]Barchuk AR, Cristino AS, Kucharski R, Costa LF, Simoes ZLP, Maleszka R: Molecular determinants of caste differentiation in the highly eusocial honeybee Apis mellifera. BMC Dev Biol 2007, 7:70. BioMed Central Full Text
• [52]Evans JD, Wheeler DE: Expression profiles during honeybee caste determination. Genome Biol 2001, 2:research0001-research0001.6.
• [53]Wilson MJ, Dearden PK: RNA localization in the honeybee (Apis mellifera) oocyte reveals insights about the evolution of RNA localization mechanisms. Dev Biol 2013, 375:193-201.
• [54]Cardoen D, Ernst UR, Boerjan B, Bogaerts A, Formesyn E, de Graaf DC, Wenseleers T, Schoofs L, Verleyen P: Worker honeybee sterility: a proteomic analysis of suppressed ovary activation. J Proteome Res 2012, 11:2838-2850.
• [55]Magie CR, Parkhurst SA: Rho1 regulates signaling events required for proper Drosophila embryonic development. Dev Biol 2005, 278:144-154.
• [56]Fu C, Whitfield CW: Genes associated with honey bee behavioral maturation affect clock-dependent and -independent aspects of daily rhythmic activity in fruit flies. Plos One 2012, 7(5):e29157.
• [57]Brembeck FH, Rosario M, Birchmeier W: Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr Opin Genet Dev 2006, 16:51-59.
• [58]Cardoen D, Ernst UR, Van Vaerenbergh M, Boerjan B, de Graaf DC, Wenseleers T, Schoofs L, Verleyen P: Differential proteomics in dequeened honeybee colonies reveals lower viral load in hemolymph of fertile worker bees. Plos One 2011, 6(6):e20043.
• [59]Chandrasekaran S, Ament SA, Eddy JA, Rodriguez-Zas SL, Schatz BR, Price ND, Robinson GE: Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. Proc Natl Acad Sci U S A 2011, 108:18020-18025.
• [60]Clough E, Moon W, Wang SX, Smith K, Hazelrigg T: Histone methylation is required for oogenesis in Drosophila. Development 2007, 134:157-165.
• [61]Luscombe NM, Babu MM, Yu HY, Snyder M, Teichmann SA, Gerstein M: Genomic analysis of regulatory network dynamics reveals large topological changes. Nature 2004, 431:308-312.
• [62]Flatt T, Tu MP, Tatar M: Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 2005, 27:999-1010.
• [63]LaFever L, Drummond-Barbosa D: Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 2005, 309:1071-1073.
• [64]Ament SA, Corona M, Pollock HS, Robinson GE: Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc Natl Acad Sci U S A 2008, 105:4226-4231.
• [65]Brody T: The interactive fly: gene networks, development and the internet. Trends Genet 1999, 15:333-334.
• [66]Hartfelder K, Kostlin K, Hepperle C: Ecdysteroid-dependent protein-synthesis in caste-specific development of the larval honey-bee ovary. Roux Arch Dev Biol 1995, 205:73-80.
• [67]Vergoz V, Lim J, Oldroyd BP: Biogenic amine receptor gene expression in the ovarian tissue of the honey bee Apis mellifera. Insect Mol Biol 2012, 21:21-29.
• [68]McQuillan HJ, Barron AB, Mercer AR: Age- and behaviour-related changes in the expression of biogenic amine receptor genes in the antennae of honey bees (Apis mellifera). J Comp Physiol A 2012, 198:753-761.
• [69]Beggs KT, Mercer AR: Dopamine receptor activation by honey bee queen pheromone. Curr Biol 2009, 19:1206-1209.
• [70]Beggs KT, Glendining KA, Marechal NM, Vergoz V, Nakamura I, Slessor KN, Mercer AR: Queen pheromone modulates brain dopamine function in worker honey bees. Proc Natl Acad Sci U S A 2007, 104:2460-2464.
• [71]Sasaki K, Nagao T: Distribution and levels of dopamine and its metabolites in brains of reproductive workers in honeybees. J Insect Physiol 2001, 47:1205-1216.
• [72]Wang Y, Amdam GV, Rueppell O, Wallrichs MA, Fondrk MK, Kaftanoglu O, Page RE: PDK1 and HR46 gene homologs tie social behavior to ovary signals. Plos One 2009, 4:4-e4899.
• [73]Hodin J, Riddiford LM: The ecdysone receptor and ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Dev Genes Evol 1998, 208:304-317.
• [74]Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE: Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proc Natl Acad Sci U S A 2007, 104:7128-7133.
• [75]Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML, Zhou Y, Partridge L, Harshman LG: Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico(1) insulin signaling mutation is autonomous to the ovary. J Insect Physiol 2005, 51:455-464.
• [76]Wu Q, Brown MR: Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 2006, 51:1-24.
• [77]Tanaka ED, Hartfelder K: The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Struct Dev 2004, 33:431-442.
• [78]Toth AL, Robinson GE: Evo-devo and the evolution of social behavior. Trends Genet 2007, 23:334-341.
• [79]Dawkins R: The selfish gene. Oxford: Oxford University Press; 1976.
• [80]Hamilton WD: The evolution of altruistic behavior. Am Nat 1963, 97:354-356.
• [81]Thompson GJ, Hurd PL, Crespi BJ: Genes underlying altruism. Biol Lett 2013, 9:20130395.