Development of a Nasonia vitripennis outbred laboratory population for genetic analysis

Molecular Ecology Resources

Volumn 14, Issue 3, 2014, Pages 578-587

  Van de Zande, Louis ^a   Ferber, Steven ^a   De Haan, Ammerins ^a   Beukeboom, Leo W ^a   Van Heerwaarden, Joost ^b   Pannebakker, Bart A ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Effective population size; Genetic variation; Laboratory strain; Parasitoid wasp; Pooled resequencing; Single nucleotide polymorphism (SNP)

Indexed keywords

ANIMAL; BREEDING; CLASSIFICATION; EXPERIMENTAL ANIMAL; FEMALE; GENETIC VARIABILITY; GENETICS; GENOME; MALE; OUTBRED STRAIN; WASP;

ANIMALS; ANIMALS, LABORATORY; ANIMALS, OUTBRED STRAINS; BREEDING; FEMALE; GENETIC VARIATION; GENOME; MALE; WASPS;

EID: 84898470300     PISSN: 1755098X     EISSN: 17550998     Source Type: Journal    
DOI: 10.1111/1755-0998.12201     Document Type: Article

References (86)

1. Bartlett AC (1993) Maintaining genetic diversity in laboratory colonies of parasites and predators. In: Applications of Genetics to Arthropods of Biological Control Significance (eds Narang S, Bartlett A, Faust R), pp. 133-145. CRC Press, Boca Raton, FL.
2. Begun DJ, Aquadro C (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature, 356, 519-520.
3. Beukeboom LW, van den Assem J (2004) A review of Nasonia (Chalcidoidea, Pteromalidae) courtship and mating behaviour, with some additional new observations. Proceedings of the section Experimental and Applied Entomology of the Netherlands Entomological Society, 15, 123-132.
4. Beukeboom LW, Niehuis O, Pannebakker BA et al. (2010) A comparison of recombination frequencies in intraspecific versus interspecific mapping populations of Nasonia. Heredity, 104, 302-309.
5. Bordenstein SR, Werren JH (2007) Bidirectional incompatibility among divergent Wolbachia and incompatibility level differences among closely related Wolbachia in Nasonia. Heredity, 99, 278-287.
6. Bordenstein SRR, O'Hara FPP, Werren JH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature, 409, 707-710.
7. Briscoe DA, Malpica JM, Robertson A et al. (1992) Rapid loss of genetic variation in large captive populations of Drosophila flies: implications for the genetic management of captive populations. Conservation Biology, 6, 416-425.
8. Brown S (2010) The Nasonia genome sequence: finding gems in the jewel (wasp) box. Insect Molecular Biology, 19, v-vii.
9. Brucker RM, Bordenstein SR (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science, 341, 667-669.
10. Burke MK, Dunham JP, Shahrestani P et al. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature, 467, 587-590.
11. Davies I (1975) A study of the effect of diet on the life-span of Nasonia vitripennis (Walk.) (Hymenoptera, Pteromalidae). Journal of Gerontology, 30, 294-298.
12. Desjardins CA, Perfectti F, Bartos JD, Enders LS, Werren JH (2010) The genetic basis of interspecies host preference differences in the model parasitoid Nasonia. Heredity, 104, 270-277.
13. Desjardins CA, Gadau J, Lopez JA et al. (2013) Fine-scale mapping of the Nasonia genome to chromosomes using a high-density genotyping microarray. G3 (Bethesda), 3, 205-215.
14. Desplan C, Beukeboom LW (2003) Nasonia. Current Biology, 13, R860.
15. Drapeau MD, Werren JH (1999) Differences in mating behaviour and sex ratio between three sibling species of Nasonia. Evolutionary Ecology Research, 1, 223-234.
16. Falconer DS, Mackay TFC (1996) Introduction to Quantitative Genetics. Longmans Green, Harlow, Essex, UK.
17. Frankham R (1995) Conservation genetics. Annual Review of Genetics, 29, 305-327.
18. Gadau J, Wolschin F (2009) Deciphering proteomic signatures of early diapause in Nasonia. PLoS ONE, 4, e6394.
19. Gadau J, Page REE, Werren JH et al. (1999) Mapping of hybrid incompatibility loci in Nasonia. Genetics, 153, 1731-1741.
20. Geuverink E, Gerritsma S, Pannebakker BA, Beukeboom LW (2009) A role for sexual conflict in the evolution of reproductive traits in Nasonia wasps? Animal Biology, 59, 417-434.
21. Gibson JD, Niehuis O, Peirson BRE, Cash EI, Gadau J (2013) Genetic and developmental basis of F2 hybrid breakdown in Nasonia parasitoid wasps. Evolution, 67, 2124-2132.
22. Godfray HCJ (2010) Nasonia: a jewel among wasps. Heredity, 104, 235-236.
23. Gokhman VE, Westendorff M (2000) The chromosomes of three species of the Nasonia complex (Hymenoptera, Pteromalidae). Beiträge zur Entomologie, 50, 193-198.
24. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices. Available from http://www2.unil.ch/popgen/softwares/fstat.htm.
25. Gregory TR (2013) Animal Genome Size Database. Available from http://www.genomesize.com.
26. Grillenberger BK, Gadau J, Bijlsma R, van de Zande L, Beukeboom LW (2009a) Female dispersal and isolation-by-distance of Nasonia vitripennis populations in a local mate competition context. Entomologia Experimentalis et Applicata, 132, 147-154.
27. Grillenberger BK, van de Zande L, Bijlsma R, Gadau J, Beukeboom LW (2009b) Reproductive strategies under multiparasitism in natural populations of the parasitoid wasp Nasonia (Hymenoptera). Journal of Evolutionary Biology, 22, 460-470.
28. Hedrick PW, Parker JD (1997) Evolutionary genetics and genetic variation of haplodiploids and X-linked genes. Annual Review of Ecology and Systematics, 28, 55-83.
29. Huang W, Richards S, Carbone MA et al. (2012) Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proceedings of the National Academy of Sciences of the United States of America, 109, 15553-15559.
30. King BH (1993) Flight activity in the parasitoid wasp Nasonia vitripennis (Hymenoptera, Pteromalidae). Journal of Insect Behavior, 6, 313-321.
31. Koboldt DC, Zhang Q, Larson DE et al. (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Research, 22, 568-576.
32. Koevoets T, Niehuis O, van de Zande L, Beukeboom LW (2012) Hybrid incompatibilities in the parasitic wasp genus Nasonia: negative effects of hemizygosity and the identification of transmission ratio distortion loci. Heredity, 108, 302-311.
33. Kofler R, Orozco-terWengel P, De Maio N et al. (2011) PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. (M Kayser, Ed.) PLoS ONE, 6, e15925.
34. Kover PX, Valdar W, Trakalo J et al. (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana. PLoS Genetics, 5, e1000551.
35. Lalonde RG (2005) Egg size variation does not affect offspring performance under intraspecific competition in Nasonia vitripennis, a gregarious parasitoid. Journal of Animal Ecology, 74, 630-635.
36. Legner E, Gerling D (1967) Host-feeding and oviposition on Musca domestica by Spalangia cameroni, Nasonia vitripennis, and Muscidifurax raptor (Hymenoptera: Pteromalidae) influences their longevity and fecundity. Annals of the Entomological Society of America, 60, 678-691.
37. Loehlin DW, Werren JH (2012) Evolution of shape by multiple regulatory changes to a growth gene. Science, 335, 943-947.
38. Loehlin DW, Enders LS, Werren JH (2010a) Evolution of sex-specific wing shape at the widerwing locus in four species of Nasonia. Heredity, 104, 260-269.
39. Loehlin DW, Oliveira DCSG, Edwards R et al. (2010b) Non-coding changes cause sex-specific wing size differences between closely related species of Nasonia. PLoS Genetics, 6, e1000821.
40. Lynch JA, Ozüak O, Khila A et al. (2011) The phylogenetic origin of oskar coincided with the origin of maternally provisioned germ plasm and pole cells at the base of the Holometabola. PLoS genetics, 7, e1002029.
41. Mackay TFC, Richards S, Stone EA et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature, 482, 173-178.
42. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, New York.
43. Marjoram P, Molitor J, Plagnol V, Tavare S (2003) Markov chain Monte Carlo without likelihoods. Proceedings of the National Academy of Sciences of the United States of America, 100, 15324-15328.
44. Muers M (2010) Evo-devo: Nasonia tools up. Nature Reviews Genetics, 11, 170-171.
45. Munoz-Torres MC, Reese JT, Childers CP et al. (2011) Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Research, 39, D658-D662.
46. Nachman M (2002) Variation in recombination rate across the genome: evidence and implications. Current Opinion in Genetics & Development, 12, 657-663.
47. Nicholson G, Smith AV, Jonsson F et al. (2002) Assessing population differentiation and isolation from single-nucleotide polymorphism data. Journal of the Royal Statistical Society Series B-Statistical Methodology, 64, 695-715.
48. Niehuis O, Gibson JD, Rosenberg MS et al. (2010) Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE, 5, e8597.
49. Niehuis O, Buellesbach J, Gibson JD et al. (2013) Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature, 494, 7-10.
50. Nunney L (2003) Managing captive populations for release: a population genetic perspective. In: Quality Control and Production of Biological Control Agents: Theory and Testing Procedures (ed. van Lenteren JC), pp. 73-97. CAB International, Wallingford, UK.
51. Orozco-terWengel P, Kapun M, Nolte V et al. (2012) Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles. Molecular Ecology, 21, 4931-4941.
52. Pannebakker BA, Halligan DLDL, Reynolds KTT et al. (2008) Effects of spontaneous mutation accumulation on sex ratio traits in a parasitoid wasp. Evolution, 62, 1921-1935.
53. Pannebakker BA, Niehuis O, Hedley A, Gadau J, Shuker DM (2010) The distribution of microsatellites in the Nasonia parasitoid wasp genome. Insect Molecular Biology, 19, 91-98.
54. Pannebakker BA, Watt R, Knott SA, West SA, Shuker DM (2011) The quantitative genetic basis of sex ratio variation in Nasonia vitripennis: a QTL study. Journal of Evolutionary Biology, 24, 12-22.
55. Paolucci S, van de Zande L, Beukeboom LW (2013) Adaptive latitudinal cline of photoperiodic diapause induction in the parasitoid Nasonia vitripennis in Europe. Journal of Evolutionary Biology, 26, 705-718.
56. Pritchard JK, Seielstad MT, Perez-Lezaun A, Feldman MW (1999) Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Molecular Biology and Evolution, 16, 1791-1798.
57. Pultz MA, Zimmerman KK, Alto NM et al. (2000) A genetic screen for zygotic embryonic lethal mutations affecting cuticular morphology in the wasp Nasonia vitripennis. Genetics, 154, 1213-1229.
58. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org/.
59. Raychoudhury R, Desjardins CA, Buellesbach J et al. (2010a) Behavioral and genetic characteristics of a new species of Nasonia. Heredity, 104, 278-288.
60. Raychoudhury R, Grillenberger BK, Gadau J et al. (2010b) Phylogeography of Nasonia vitripennis (Hymenoptera) indicates a mitochondrial-Wolbachia sweep in North America. Heredity, 104, 318-326.
61. Rivero A, West SA (2002) The physiological costs of being small in a parasitic wasp. Evolutionary Ecology Research, 4, 407-420.
62. Rivero A, West SA (2005) The costs and benefits of host feeding in parasitoids. Animal Behaviour, 69, 1293-1301.
63. Rivers DB, Denlinger DL (1995) Fecundity and development of the ectoparasitic wasp Nasonia vitripennis are dependent on host quality. Entomologia Experimentalis et Applicata, 76, 15-24.
64. Rivers DBDB, Kaikis A, Bulanowski D, Wigand T, Brogan R (2012) Oviposition restraint and developmental alterations in the ectoparasitic wasp, Nasonia vitripennis, when utilizing puparia resulting from different size maggot masses of Lucilia illustris, Protophormia terraenovae, and Sarcophaga bullata. Journal of Medical Entomology, 49, 1124-1136.
65. Roush R (1990) Genetic variation in natural enemies: critical issues for colonization in biological control. In: Critical Issues in Biological Control (eds Mackauer M, Ehler L, Roland J), pp. 263-288. Intercept, Andover, UK.
66. Shuker DM, West SA (2004) Information constraints and the precision of adaptation: sex ratio manipulation in wasps. Proceedings of the National Academy of Sciences of the United States of America, 101, 10363-10367.
67. Shuker DM, Pen I, Duncan AB, Reece SE, West SA (2005) Sex ratios under asymmetrical local mate competition: theory and a test with parasitoid wasps. The American Naturalist, 166, 301-316.
68. Shuker DM, Phillimore AJ, Burton-Chellew MN, Hodge SE, West SA (2007a) The quantitative genetic basis of polyandry in the parasitoid wasp, Nasonia vitripennis. Heredity, 98, 69-73.
69. Shuker DM, Reece SE, Lee A et al. (2007b) Information use in space and time: sex allocation behaviour in the parasitoid wasp Nasonia vitripennis. Animal Behaviour, 73, 971-977.
70. Simoes P, Pascual M, Coelho M, Matos M (2010) Divergent evolution of molecular markers during laboratory adaptation in Drosophila subobscura. Genetica, 138, 999-1009.
71. Smith GJC, Pimentel D (1969) The effect of two host species on the longevity and fertility of Nasonia vitripennis. Annals of the Entomological Society of America, 62, 305-308.
72. Svenson KL, Gatti DM, Valdar W et al. (2012) High-resolution genetic mapping using the Mouse Diversity outbred population. Genetics, 190, 437-447.
73. Tavare S, Balding D, Griffiths R, Donnelly P (1997) Inferring coalescence times from DNA sequence data. Genetics, 145, 505-518.
74. Verhulst EC, Beukeboom LW, van de Zande L (2010) Maternal control of haplodiploid sex determination in the wasp Nasonia. Science, 328, 620-623.
75. Wang X, Wheeler D, Avery A et al. (2013) Function and evolution of DNA methylation in Nasonia vitripennis. PLoS genetics, 9, e1003872.
76. Weber K (2004) Population size and long-term selection. (J Janick, Ed.) Plant Breeding Reviews, 24, 249-268.
77. Weber KE, Diggins LT (1990) Increased selection response in larger populations. II. Selection for ethanol vapor resistance in Drosophila melanogaster at two population sizes. Genetics, 125, 585-597.
78. Werren JH (1980) Sex ratio adaptations to local mate competition in a parasitic wasp. Science, 208, 1157-1159.
79. Werren JH (1983a) Sex ratio evolution under local mate competition in a parasitic wasp. Evolution, 37, 116-124.
80. Werren JH (1983b) Brood size and sex ratio regulation in the parasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). Netherlands Journal of Zoology, 34, 123-143.
81. Werren JH, Loehlin DW (2009) The parasitoid wasp Nasonia: an emerging model system with haploid male genetics. Cold Spring Harbor Protocols, 10, doi: 10.1101/pdb.emo134.
82. Werren JH, Richards S, Desjardins CA et al. (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science, 327, 343-348.
83. Whiting AR (1967) The biology of the parasitic wasp Mormoniella vitripennis (Walker). Quarterly Review of Biology, 42, 333-406.
84. Wright S (1933) Inbreeding and homozygosis. Proceedings of the National Academy of Sciences of the United States of America, 19, 411-420.
85. Wylie HG (1966) Survival and reproduction of Nasonia vitripennis (Walk) at different host population densities. The Canadian Entomologist, 98, 275-281.
86. Zhang X-S, Hill WG (2005) Predictions of patterns of response to artificial selection in lines derived from natural populations. Genetics, 169, 411-425.