期刊论文详细信息
BMC Evolutionary Biology
Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.)
Olav Rueppell1  Gro V Amdam4  Robert E Page2  Osman Kaftanoglu2  Michael D Munday1  Allie M Graham3 
[1] Department of Biology, University of North Carolina at Greensboro, 1000 Spring Garden Street, 312 Eberhart Building, Greensboro, NC, 27403, USA;School of Life Sciences, Arizona State University, PO Box 874501, Tempe, AZ 85287-4501, USA;Current address: Duke University, Department of Biology, Box 90338 Durham, NC 27708, USA;Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Aas, Norway
关键词: Asymmetry;    Worker reproduction;    Pollen hoarding syndrome;    Complex trait locus mapping;    Social evolution;    Reproductive groundplan hypothesis;   
Others  :  1144647
DOI  :  10.1186/1471-2148-11-95
 received in 2010-11-29, accepted in 2011-04-13,  发布年份 2011
PDF
【 摘 要 】

Background

The reproductive ground plan hypothesis of social evolution suggests that reproductive controls of a solitary ancestor have been co-opted during social evolution, facilitating the division of labor among social insect workers. Despite substantial empirical support, the generality of this hypothesis is not universally accepted. Thus, we investigated the prediction of particular genes with pleiotropic effects on ovarian traits and social behavior in worker honey bees as a stringent test of the reproductive ground plan hypothesis. We complemented these tests with a comprehensive genome scan for additional quantitative trait loci (QTL) to gain a better understanding of the genetic architecture of the ovary size of honey bee workers, a morphological trait that is significant for understanding social insect caste evolution and general insect biology.

Results

Back-crossing hybrid European x Africanized honey bee queens to the Africanized parent colony generated two study populations with extraordinarily large worker ovaries. Despite the transgressive ovary phenotypes, several previously mapped QTL for social foraging behavior demonstrated ovary size effects, confirming the prediction of pleiotropic genetic effects on reproductive traits and social behavior. One major QTL for ovary size was detected in each backcross, along with several smaller effects and two QTL for ovary asymmetry. One of the main ovary size QTL coincided with a major QTL for ovary activation, explaining 3/4 of the phenotypic variance, although no simple positive correlation between ovary size and activation was observed.

Conclusions

Our results provide strong support for the reproductive ground plan hypothesis of evolution in study populations that are independent of the genetic stocks that originally led to the formulation of this hypothesis. As predicted, worker ovary size is genetically linked to multiple correlated traits of the complex division of labor in worker honey bees, known as the pollen hoarding syndrome. The genetic architecture of worker ovary size presumably consists of a combination of trait-specific loci and general regulators that affect the whole behavioral syndrome and may even play a role in caste determination. Several promising candidate genes in the QTL intervals await further study to clarify their potential role in social insect evolution and the regulation of insect fertility in general.

【 授权许可】

   
2011 Graham et al; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150330221223411.pdf 363KB PDF download
Figure 5. 45KB Image download
Figure 4. 40KB Image download
Figure 3. 116KB Image download
Figure 2. 80KB Image download
Figure 1. 14KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Amdam GV, Csondes A, Fondrk MK, Page RE: Complex social behaviour derived from maternal reproductive traits. Nature 2006, 439:76-78.
  • [2]Amdam GV, Norberg K, Fondrk MK, Page RE Jr: Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc Nat Acad Sci USA 2004, 101:11350-11355.
  • [3]Page RE, Scheiner R, Erber J, Amdam GV: The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr Top Developm Biol 2007, 74:253-286.
  • [4]West-Eberhard MJ: Flexible Strategy and Social Evolution. In Animal Societies, Theories and Facts. Edited by Ito Y, Brown JL, Kikkawa J. Tokyo: Japan Scientific Societies Press; 1987:35-51.
  • [5]West-Eberhard MJ: Wasp societies as microcosms for the study of development and evolution. In Natural History and Evolution of Paper Wasps. Edited by Turillazzi S, West-Eberhard MJ. New York: Oxford University Press; 1996:290-317.
  • [6]Wang Y, Amdam GV, Rueppell O, Wallrichs MA, Fondrk MK, Kaftanoglu O, Page RE Jr: PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS ONE 2009, 4:e4899.
  • [7]Rueppell O, Hunggims E, Tingek S: Association between larger ovaries and pollen foraging in queenless Apis cerana workers supports the reproductive ground - plan hypothesis of social evolution. Journal of Insect Behavior 2008, 21:317-321.
  • [8]Page RE, Amdam GV: The making of a social insect: developmental architectures of social design. Bioessays 2007, 29:334-343.
  • [9]Tsuruda JM, Amdam GV, Page RE: Sensory response system of social behavior tied to female reproductive traits. PLoS ONE 2008, 3:5.
  • [10]Oldroyd BP, Beekman M: Effects of selection for honey bee worker reproduction on foraging traits. Plos Biology 2008, 6:e56.
  • [11]Amdam GV, Nilsen KA, Norberg K, Fondrk MK, Hartfelder K: Variation in endocrine signaling underlies variation in social life history. American Naturalist 2007, 170:37-46.
  • [12]Amdam GV, Norberg K, Page RE, Erber J, Scheiner R: Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera). Behavioral Brain Research 2006, 169:201-205.
  • [13]Nelson CM, Ihle KE, Fondrk MK, Page RE Jr, Amdam GV: The gene vitellogenin has multiple coordinating effects on social organization. Plos Biology 2007, 5:e62.
  • [14]Wang Y, Mutti NS, Ihle KE, Siegel A, Dolezal AG, Kaftanoglu O, Amdam GV: Down-regulation of honey bee IRS gene biases behavior toward food rich in protein. PLoS Genet 2010, 6:e1000896.
  • [15]Oldroyd BP, Fewell JH: Genetic diversity promotes homeostasis in insect colonies. Trends in Ecology & Evolution 2007, 22:408-413.
  • [16]Makert GR, Paxton RJ, Hartfelder K: Ovariole number - a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies. Behav Ecol Sociobiol 2006, 60:815-825.
  • [17]Page RE, Fondrk MK: The effects of colony level selection on the social organization of honey bee (Apis mellifera L) colonies - colony level components of pollen hoarding. Behav Ecol Sociobiol 1995, 36:135-144.
  • [18]Schneider SS, DeGrandi-Hoffman G, Smith DR: The African honey bee: Factors contributing to a successful biological invasion. Annu Rev Entomol 2004, 49:351-376.
  • [19]Whitfield CW, Behura SK, Berlocher SH, Clark AG, Johnston JS, Sheppard WS, Smith DR, Suarez AV, Weaver D, Tsutsui ND: Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 2006, 314:642-645.
  • [20]Pankiw T: Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (Apis mellifera L.). Behav Ecol Sociobiol 2003, 54:458-464.
  • [21]Ruttner F, Hesse B: Specific differences in the development of ovaries and egg-laying of queenless workers of several races of the honeybee, Apis mellifera L. Apidologie 1981, 12:159-183.
  • [22]Linksvayer TA, Rueppell O, Siegel A, Kaftanoglu O, Page RE Jr, Amdam GV: The genetic basis of transgressive ovary size in honey bee workers. Genetics 2009, 183:693-707.
  • [23]Thuller RHC, Malaspina O, Bueno OC, Chaud-Netto J: Number of ovarioles in workers descendent from crossing between Africanized and Italian honeybees (Apis mellifera L.): Comparing stock, inbred and F1 colonies. Anais da Sociedade Entomologica do Brasil 1996, 25:501-506.
  • [24]Page RE, Fondrk MK, Hunt GJ, Guzman-Novoa E, Humphries MA, Nguyen K, Greene AS: Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. Journal of Heredity 2000, 91:474-479.
  • [25]Hunt GJ, Page RE Jr, Fondrk MK, Dullum CJ: Major quantitative trait loci affecting honey bee foraging behavior. Genetics 1995, 141:1537-1545.
  • [26]Rüppell O, Pankiw T, Page RE Jr: Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. Journal of Heredity 2004, 95:481-491.
  • [27]Rueppell O, Chandra SBC, Pankiw T, Fondrk MK, Beye M, Hunt GJ, Page RE: The genetic architecture of sucrose responsiveness in the honey bee (Apis mellifera L.). Genetics 2006, 172:243-251.
  • [28]Rueppell O, Pankiw T, Nielson DI, Fondrk MK, Beye M, Page RE Jr: The genetic architecture of the behavioral ontogeny of foraging in honey bee workers. Genetics 2004, 167:1767-1779.
  • [29]Hunt GJ, Amdam GV, Schlipalius D, Emore C, Sardesai N, Williams CE, Rueppell O, Guzman-Novoa E, Arechavaleta-Velasco M, Chandra S, et al.: Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 2007, 94:247-267.
  • [30]Rueppell O: Characterization of quantitative trait loci for the age of first foraging in honey bee workers. Behavior Genetics 2009, 39:541-553.
  • [31]Bergland AO, Genissel A, Nuzhdin SV, Tatar M: Quantitative trait loci affecting phenotypic plasticity and the allometric relationship of ovariole number and thorax length in Drosophila melanogaster. Genetics 2008, 180:567-582.
  • [32]Orgogozo V, Broman KW, Stern DL: High-resolution quantitative trait locus mapping reveals sign epistasis controlling ovariole number between two Drosophila species. Genetics 2006, 173:197-205.
  • [33]Wayne ML, Hackett JB, Dilda CL, Nuzhdin SV, Pasyukova EG, MacKay TFC: Quantitative trait locus mapping of fitness-related traits in Drosophila melanogaster. Genetical Research 2001, 77:107-116.
  • [34]Hartfelder K, Engels W: Social insect polymorphism: Hormonal regulation of plasticity in development and reproduction in the honeybee. Current Topics in Developmental Biology 1998, 40:45-77.
  • [35]Phiancharoen M, Pirk CWW, Radloff SE, Hepburn R: Clinal nature of the frequencies of ovarioles and spermathecae in Cape worker honeybees, Apis mellifera capensis. Apidologie 2010, 41:129-134.
  • [36]Rueppell O, Metheny JD, Linksvayer TA, Fondrk MK, Page RE Jr, Amdam GV: Genetic architecture of ovary size and asymmetry in European honey bee workers. Heredity, in press.
  • [37]Amdam GV, Page RE: The developmental genetics and physiology of honeybee societies. Animal Behaviour 2010, 79:973-980.
  • [38]Schmidt Capella IC, Hartfelder K: Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. Journal of Insect Physiology 1998, 44:385-391.
  • [39]Schmidt Capella IC, Hartfelder K: Juvenile-hormone-dependent interaction of actin and spectrin is crucial for polymorphic differentiation of the larval honey bee ovary. Cell and Tissue Research 2002, 307:265-272.
  • [40]Mahajanmiklos S, Cooley L: The villin-like protein encoded by the Drosophila quail gene is required for actin bundle assembly during oogenesis. Cell 1994, 78:291-301.
  • [41]Guertin DA, Guntur KVP, Bell GW, Thoreen CC, Sabatini DM: Functional Genomics identifies TOR-regulated genes that control growth and division. Current Biology 2006, 16:958-970.
  • [42]Beckstead RB, Lam G, Thummel CS: The genomic response to 20-hydroxyecdysone at the onset of Drosophila metamorphosis. Genome Biol 2005, 6:R99. BioMed Central Full Text
  • [43]Munoz-Descalzo S, Terol J, Paricio N: Cabut, a C2H2 zinc finger transcription factor, is required during Drosophila dorsal closure downstream of JNK signaling. Dev Biol 2005, 287:168-179.
  • [44]Gorski SM, Chittaranjan S, Pleasance ED, Freeman JD, Anderson CL, Varhol RJ, Coughlin SM, Zuyderduyn SD, Jones SJ, Marra MA: A SAGE approach to discovery of genes involved in autophagic cell death. Curr Biol 2003, 13:358-363.
  • [45]Wang Y, Kocher SD, Linksvayer TA, Grozinger C, Page RE Jr, Amdam GV: Regulation of behaviorally-associated gene pathways in worker honey bee ovaries. Bmc Genetics, in press.
  • [46]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 Developmental Biology 2007, 7:70. BioMed Central Full Text
  • [47]Zelhof AC, Yao TP, Chen JD, Evans RM, McKeown M: Seven-up inhibits ultraspiracle-based signaling pathways in vitro and in vivo. Mol Cell Biol 1995, 15:6736-6745.
  • [48]Kerber B, Fellert S, Hoch M: Seven-up, the Drosophila homolog of the COUP-TF orphan receptors, controls cell proliferation in the insect kidney. Genes Dev 1998, 12:1781-1786.
  • [49]Kanai MI, Okabe M, Hiromi Y: Seven-up controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Dev Cell 2005, 8:203-213.
  • [50]Shpigler H, Patch HM, Cohen M, Fan Y, Grozinger CM, Bloch G: The transcription factor Kruppel homolog 1 is linked to hormone mediated social organization in bees. BMC Evol Biol 2010, 10:120. BioMed Central Full Text
  • [51]Velthuis HHW, Clement JL, Morse RA, Laigo FM: The ovaries of Apis dorsata from the Philippines. Journal of Apicultural Research 1971, 10:63-66.
  • [52]Das Thakur M, Feng Y, Jagannathan R, Seppa MJ, Skeath JB, Longmore GD: Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr Biol 2010, 20:657-662.
  • [53]Buszczak M, Lu X, Segraves WA, Chang TY, Cooley L: Mutations in the midway gene disrupt a Drosophila acyl coenzyme A: diacylglycerol acyltransferase. Genetics 2002, 160:1511-1518.
  • [54]Linksvayer TA: Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant. Evolution 2006, 60:2552-2561.
  • [55]Wong AH, Gottesman II, Petronis A: Phenotypic differences in genetically identical organisms: the epigenetic perspective. Hum Mol Genet 2005, 14(1):R11-18.
  • [56]Palmer AR, Strobeck C: Fluctuating asymmetry - measurement, analysis, patterns. Annual Review of Ecology and Systematics 1986, 17:391-421.
  • [57]Chaud-Netto J, Bueno OC: Number of ovarioles in workers of Apis mellifera adansonii and Apis mellifera ligustica: a comparative study. Journal of Apicultural Research 1979, 18:260-263.
  • [58]Leamy LJ, Routman EJ, Cheverud JM: A search for quantitative trait loci affecting asymmetry of mandibular characters in mice. Evolution 1997, 51:957-969.
  • [59]Oxley PR, Thompson GJ, Oldroyd BP: Four quantitative trait loci that influence worker sterility in the honeybee (Apis mellifera). Genetics 2008, 179:1337-1343.
  • [60]Schafer MO, Dietemann V, Pirk CWW, Neumann P, Crewe RM, Hepburn HR, Tautz J, Crailsheim K: Individual versus social pathway to honeybee worker reproduction (Apis mellifera): pollen or jelly as protein source for oogenesis? J Comp Physiol A 2006, 192:761-768.
  • [61]Page RE, Erickson EH: Reproduction by worker honey bees (Apis mellifera L). Behav Ecol Sociobiol 1988, 23:117-126.
  • [62]Pernal SF, Currie RW: Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.). Apidologie 2000, 31:387-409.
  • [63]Ragoussis J, Elvidge GP, Kaur K, Colella S: Matrix-assisted laser desorption/ionisation, time-of-flight mass spectrometry in genomics research. Plos Genetics 2006, 2:920-929.
  • [64]Solignac M, Mougel F, Vautrin D, Monnerot M, Cornuet JM: A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biology 2007, 8:R66. BioMed Central Full Text
  • [65]The Honey Bee Genome Consortium: Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443:931-949.
  • [66]Schuelke M: An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 2000, 18:233-234.
  • [67]Schug MD, Regulski EE, Pearce A, Smith SG: Isolation and characterization of dinucleotide repeat microsatellites in Drosophila ananassae. Genetical Research 2004, 83:19-29.
  • [68]Lincoln SE, Daly MJ, Lander ES: Constructing Genetic Linkage Maps with MAPMAKER/EXP Version 3.0: A Tutorial and Reference Manual. A Whitehead Institute for Biomedical Research Technical Report. Cambridge, MA 1993.
  • [69]Van Ooijen JW, Boer MP, Jansen RC, Maliepaard C: MapQTL 4.0, Software for the calculation of QTL positions on genetic maps. Plant Research International, Wageningen, the Netherlands; 2002.
  • [70]Churchill GA, Doerge RW: Empirical threshold values for quantitative trait mapping. Genetics 1994, 138:963-971.
  文献评价指标  
  下载次数:111次 浏览次数:61次