Pleiotropy of segregating genetic variants that affect honey bee worker life expectancy

Experimental Gerontology

Volumn 47, Issue 8, 2012, Pages 631-637

  Dixon, Luke R ^a   McQuage, Michelle R ^a   Lonon, Ellen J ^a   Buehler, Dominique ^a,b   Seck, Oumar ^a   Rueppell, Olav ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^b Schnee und Landschaft ^*  (Switzerland)

Author keywords

Division of labor; Genetic architecture; Lifespan; Longevity; Pleiotropy; QTL; Social evolution

Indexed keywords

GENOMIC DNA;

AGE DISTRIBUTION; ANIMAL BEHAVIOR; ARTICLE; BACKCROSSING; FEMALE; GENE LOCATION; GENE SEGREGATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOME ANALYSIS; HONEYBEE; LIFE EXPECTANCY; LONGEVITY; MALE; MICROSATELLITE MARKER; NONHUMAN; PLEIOTROPY; POLLEN HOARDING SYNDROME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS MAPPING; SINGLE NUCLEOTIDE POLYMORPHISM; SOCIAL EVOLUTION; SURVIVAL; WORKER (INSECT);

AGING; ANIMALS; BEES; BEHAVIOR, ANIMAL; GENE FREQUENCY; GENETIC PLEIOTROPY; GENETIC VARIATION; GENOTYPE; LIFE EXPECTANCY; MICROSATELLITE REPEATS; POLLEN; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

APIS MELLIFERA; APOIDEA;

EID: 84863086359     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.05.017     Document Type: Article

References (58)

1. Amdam G.V., Nilsen K.A., Norberg K., Fondrk M.K., Hartfelder K. Variation in endocrine signaling underlies variation in social life history. Am. Nat. 2007, 170:37-46.
2. Amdam G.V., Rueppell O., Fondrk M.K., Page R.E., Nelson C.M. The nurse's load: early-life exposure to brood-rearing affects behavior and lifespan in honey bees (Apis mellifera). Exp. Gerontol. 2009, 44:467-471.
3. Ayyadevara S., Ayyadevara R., Vertino A., Galecki A., Thaden J.J., Reis R.J.S. Genetic loci modulating fitness and life span in Caenorhabditis elegans: categorical trait interval mapping in CL2a X Bergerac-BO recombinant-inbred worms. Genetics 2003, 163:557-570.
4. Beye M., Hasselmann M., Fondrk M.K., Page R.E., Omholt S.W. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 2003, 114:419-429.
5. Beye M., Gattermeier I., Hasselmann M., Gempe T., Schioett M., Baines J.F., Schlipalius D., Mougel F., Emore C., Rueppell O., Sirvio A., Guzman-Novoa E., Hunt G., Solignac M., Page R.E. Exceptionally high levels of recombination across the honey bee genome. Genome Res. 2006, 16:1339-1344.
6. Carey J.R., Liedo P., Muller H.G., Wang J.L., Vaupel J.W. Dual modes of aging in Mediterranean fruit fly females. Science 1998, 281:996-998.
7. Ebert R.H., Cherkasova V.A., Dennis R.A., Wu J.H., Ruggles S., Perrin T.E., Reis R.J.S. Longevity determining genes in Caenorhabditis elegans - Chromosomal mapping of multiple noninteractive loci. Genetics 1993, 135:1003-1010.
8. Finch C.E., Kirkwood T.B.L. Chance, Development, and Aging 2000, Oxford University Press, New York.
9. Finch C.E., Tanzi R.E. Genetics of aging. Science 1997, 278:407-411.
10. Graham A.M., Munday M.D., Kaftanoglu O., Page R.E., Amdam G.V., Rueppell O. Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.). BMC Evol. Biol. 2011, 11:95.
11. Gronke S., Muller G., Hirsch J., Fellert S., Andreou A., Haase T., Jackle H., Kuhnlein R.P. Dual lipolytic control of body fat storage and mobilization in Drosophila. PLoS Biol. 2007, 5:e137.
12. Hedrick P.W., Parker J.D. Evolutionary genetics and genetic variation of haplodiploids and X-linked genes. Annu. Rev. Ecol. Syst. 1997, 28:55-83.
13. Honeybee Genome Consortium Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006, 443:931-949.
14. Hunt G.J., Page R.E. Linkage map of the honey bee, Apis mellifera, based on RAPD markers. Genetics 1995, 139:1371-1382.
15. Hunt G.J., Page R.E., Fondrk M.K., Dullum C.J. Major quantitative trait loci affecting honey bee foraging behavior. Genetics 1995, 141:1537-1545.
16. Hunt G.J., Amdam G.V., Schlipalius D., Emore C., Sardesai N., Williams C.E., Rueppell O., Guzman-Novoa E., Arechavaleta-Velasco M., Chandra S., Fondrk M.K., Beye M., Page R.E. Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 2007, 94:247-267.
17. Hurst G.D.D., Werren J.H. The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2001, 2:597-606.
18. Jackson A.U., Galecki A.T., Burke D.T., Miller R.A. Mouse loci associated with life span exhibit sex-specific and epistatic effects. J. Gerontol. A: Biol. Sci. Med. Sci. 2002, 57:B9-B15.
19. Kathiresan S., Melander O., Guiducci C., Surti A., Burtt N.P., Rieder M.J., Cooper G.M., Roos C., Voight B.F., Havulinna A.S., Wahlstrand B., Hedner T., Corella D., Tai E.S., Ordovas J.M., Berglund G., Vartiainen E., Jousilahti P., Hedblad B., Taskinen M.R., Newton-Cheh C., Salomaa V., Peltonen L., Groop L., Altshuler D.M., Orho-Melander M. Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Nat. Genet. 2008, 40:189-197.
20. Kenyon C. The plasticity of aging: insights from long-lived mutants. Cell 2005, 120:449-460.
21. Kenyon C., Chang J., Gensch E., Rudner A., Tabtiang R. A C. elegans mutant that lives twice as long as wild-type. Nature 1993, 366:461-464.
22. Lai C.Q., Leips J., Zou W., Roberts J.F., Wollenberg K.R., Parnell L.D., Zeng Z.B., Ordovas J.M., Mackay T.F.C. Speed-mapping quantitative trait loci using microarrays. Nature Methods 2007, 4:839-841.
23. Lander E.S., Schork N.J. Genetic dissection of complex traits. Science 1994, 265:2037-2048.
24. Lang D.H., Gerhard G.S., Griffith J.W., Vogler G.P., Vandenbergh D.J., Blizard D.A., Stout J.T., Lakoski J.M., McClearn G.E. Quantitative Trait Loci (QTL) analysis of longevity in C57BL/6J by DBA/2J (BXD) recombinant inbred mice. Aging Clin. Exp. Res. 2010, 22:8-19.
25. Leips J., Mackay T.F.C. Quantitative trait loci for life span in Drosophila melanogaster: interactions with genetic background and larval density. Genetics 2000, 155:1773-1788.
26. Mackay T.F.C. The genetic architecture of quantitative traits. Annu. Rev. Genet. 2001, 35:303-339.
27. Mackay T.F. The nature of quantitative genetic variation for Drosophila longevity. Mech. Ageing Dev. 2002, 123:95-104.
28. McGinnis J.M., Foege W.H. Actual causes of death in the United States. Jama J. Am. Med. Assoc. 1993, 270:2207-2212.
29. Nelson C.M., Ihle K.E., Fondrk M.K., Page R.E., Amdam G.V. The gene vitellogenin has multiple coordinating effects on social organization. Plos Biol. 2007, 5:e62.
30. Oldroyd B.P., Thompson G.J. Behavioural genetics of the honey bee Apis mellifera. Advances in Insect Physiology 2007, 33:1-49.
31. Omholt S.W., Amdam G.V. Epigenic regulation of aging in honeybee workers. Sci. Aging Knowl. Environ. 2004, 26:pe28.
32. Paaby A.B., Schmidt P.S. Dissecting the genetics of longevity in Drosophila melanogaster. Fly 2009, 3:29-38.
33. Page R.E., Fondrk M.K. 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.
34. Page R.E., Peng Y.-S.C. Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp. Gerontol. 2001, 36:695-711.
35. Page R.E., Fondrk M.K., Hunt G.J., Guzman-Novoa E., Humphries M.A., Nguyen K., Greene A.S. Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. J. Hered. 2000, 91:474-479.
36. Page R.E., Scheiner R., Erber J., Amdam G.V. The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr. Top. Dev. Biol. 2007, 74:253-286.
37. Perls T., Terry D. Genetics of exceptional longevity. Exp. Gerontol. 2003, 38:725-730.
38. Ragoussis J., Elvidge G.P., Kaur K., Colella S. Matrix-assisted laser desorption/ionisation, time-of-flight mass spectrometry in genomics research. Plos Genet. 2006, 2:920-929.
39. Rueppell O. Characterization of quantitative trait loci for the age of first foraging in honey bee workers. Behav. Genet. 2009, 39:541-553.
40. Rueppell O., Pankiw T., Nielson D.I., Fondrk M.K., Beye M., Page R.E. The genetic architecture of the behavioral ontogeny of foraging in honey bee workers. Genetics 2004, 167:1767-1779.
41. Rueppell O., Amdam G.V., Page R.E., Carey J.R. From genes to society: social insects as models for research on aging. Sci. Aging Knowl. Environ. 2004, 5. pe5.
42. Rueppell O., Chandra S.B.C., Pankiw T., Fondrk M.K., Beye M., Hunt G.J., Page R.E. The genetic architecture of sucrose responsiveness in the honey bee (Apis mellifera L.). Genetics 2006, 172:243-251.
43. Rueppell O., Bachelier C., Fondrk M.K., Page R.E. Regulation of life history determines lifespan of worker honey bees (Apis mellifera L.). Exp. Gerontol. 2007, 42:1020-1032.
44. Rueppell O., Linford R., Gardner P., Coleman J., Fine K. Aging and demographic plasticity in response to experimental age structures in honeybees (Apis mellifera L). Behav. Ecol. Sociobiol. 2008, 62:1621-1631.
45. Rüppell O., Pankiw T., Page R.E. Pleiotropy, epistasis and new QTL: the genetic architecture of honey bee foraging behavior. J. Hered. 2004, 95:481-491.
46. Schuelke M. An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 2000, 18:233-234.
47. Schug M.D., Regulski E.E., Pearce A., Smith S.G. Isolation and characterization of dinucleotide repeat microsatellites in Drosophila ananassae. Genet. Res. 2004, 83:19-29.
48. Shmookler Reis R.J., Kang P., Ayyadevara S. Quantitative trait loci define genes and pathways underlying genetic variation in longevity. Exp. Gerontol. 2006, 41:1046-1054.
49. Shook D.R., Johnson T.E. Quantitative trait loci affecting survival and fertility-related traits in Caenorhabditis elegans show genotype-environment interactions, pleiotropy and epistasis. Genetics 1999, 153:1233-1243.
50. Slagboom P.E., Beekman M., Passtoors W.M., Deelen J., Vaarhorst A.A.M., Boer J.M., van den Akker E.B., van Heemst D., de Craen A.J.M., Maier A.B., Rozing M., Mooijaart S.P., Heijmans B.T., Westendorp R.G.J. Genomics of human longevity. Philos. Trans. R. Soc. B 2011, 366:35-42.
51. Solignac M., Mougel F., Vautrin D., Monnerot M., Cornuet J.M. A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol. 2007, 8:R66.
52. Spradling A.C., Stern D., Beaton A., Rhem E.J., Laverty T., Mozden N., Misra S., Rubin G.M. The Berkeley Drosophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes. Genetics 1999, 153:135-177.
53. Tatar M., Bartke A., Antebi A. The endocrine regulation of aging by insulin-like signals. Science 2003, 299:1346-1350.
54. Wang M.H., Lazebny O., Harshman L.G., Nuzhdin S.V. Environment-dependent survival of Drosophila melanogaster: a quantitative genetic analysis. Aging Cell 2004, 3:133-140.
55. Wang Y., Amdam G.V., Rueppell O., Wallrichs M.A., Fondrk M.K., Kaftanoglu O., Page R.E. PDK1 and HR46 gene homologs tie social behavior to ovary signals. PLoS One 2009, 4:e4899.
56. Wang L., Chadwick W., Park S.S., Zhou Y., Silver N., Martin B., Maudsley S. Gonadotropin-releasing hormone receptor system: modulatory role in aging and neurodegeneration. CNS Neurol. Disord. Drug Targets 2010, 9:651-660.
57. Whitfield C.W., Behura S.K., Berlocher S.H., Clark A.G., Johnston J.S., Sheppard W.S., Smith D.R., Suarez A.V., Weaver D., Tsutsui N.D. Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 2006, 314:642-645.
58. Williams G.C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957, 11:398-411.