Abstract
There is a 2.5-fold difference in male wing size between two haplodiploid insect species, Nasonia vitripennis and N. giraulti. The haploidy of males facilitated a full genomic screen for quantitative trait loci (QTL) affecting wing size and the detection of epistatic interactions. A QTL analysis of the interspecific wing-size difference revealed QTL with major effects and epistatic interactions among loci affecting the trait. We analyzed 178 hybrid males and initially found two major QTL for wing length, one for wing width, three for a normalized wing-size variable, and five for wing seta density. One QTL for wing width explains 38.1% of the phenotypic variance, and the same QTL explains 22% of the phenotypic variance in normalized wing size. This corresponds to a region previously introgressed from N. giraulti into N. vitripennis that accounts for 44% of the normalized wing-size difference between the species. Significant epistatic interactions were also found that affect wing size and density of setae on the wing. Screening for pairwise epistatic interactions between loci on different linkage groups revealed four additional loci for wing length and four loci for normalized wing size that were not detected in the original QTL analysis. We propose that the evolution of smaller wings in N. vitripennis males is primarily the result of major mutations at few genomic regions and involves epistatic interactions among some loci.
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Selected References
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- Bordenstein S. R., O'Hara F. P., Werren J. H. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature. 2001 Feb 8;409(6821):707–710. doi: 10.1038/35055543. [DOI] [PubMed] [Google Scholar]
- Campbell B. C., Steffen-Campbell J. D., Werren J. H. Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Mol Biol. 1993;2(4):225–237. doi: 10.1111/j.1365-2583.1994.tb00142.x. [DOI] [PubMed] [Google Scholar]
- Cheverud J. M., Routman E. J. Epistasis and its contribution to genetic variance components. Genetics. 1995 Mar;139(3):1455–1461. doi: 10.1093/genetics/139.3.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Churchill G. A., Doerge R. W. Empirical threshold values for quantitative trait mapping. Genetics. 1994 Nov;138(3):963–971. doi: 10.1093/genetics/138.3.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coelho C. M., Leevers S. J. Do growth and cell division rates determine cell size in multicellular organisms? J Cell Sci. 2000 Sep;113(Pt 17):2927–2934. doi: 10.1242/jcs.113.17.2927. [DOI] [PubMed] [Google Scholar]
- Coyne J. A., Barton N. H., Turelli M. Is Wright's shifting balance process important in evolution? Evolution. 2000 Feb;54(1):306–317. doi: 10.1111/j.0014-3820.2000.tb00033.x. [DOI] [PubMed] [Google Scholar]
- Coyne J. A., Barton N. H., Turelli M. Is Wright's shifting balance process important in evolution? Evolution. 2000 Feb;54(1):306–317. doi: 10.1111/j.0014-3820.2000.tb00033.x. [DOI] [PubMed] [Google Scholar]
- Coyne J. A., Orr H. A. The evolutionary genetics of speciation. Philos Trans R Soc Lond B Biol Sci. 1998 Feb 28;353(1366):287–305. doi: 10.1098/rstb.1998.0210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Day S. J., Lawrence P. A. Measuring dimensions: the regulation of size and shape. Development. 2000 Jul;127(14):2977–2987. doi: 10.1242/dev.127.14.2977. [DOI] [PubMed] [Google Scholar]
- Fry J. D., deRonde K. A., Mackay T. F. Polygenic mutation in Drosophila melanogaster: genetic analysis of selection lines. Genetics. 1995 Mar;139(3):1293–1307. doi: 10.1093/genetics/139.3.1293. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gadau J., Page R. E., Jr, Werren J. H. Mapping of hybrid incompatibility loci in Nasonia. Genetics. 1999 Dec;153(4):1731–1741. doi: 10.1093/genetics/153.4.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodnight C. J., Wade M. J. The ongoing synthesis: a reply to Coyne, Barton, and Turelli. Evolution. 2000 Feb;54(1):317–324. doi: 10.1111/j.0014-3820.2000.tb00034.x. [DOI] [PubMed] [Google Scholar]
- Hunt G. J., Page R. E., Jr, Fondrk M. K., Dullum C. J. Major quantitative trait loci affecting honey bee foraging behavior. Genetics. 1995 Dec;141(4):1537–1545. doi: 10.1093/genetics/141.4.1537. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jansen R. C. Controlling the type I and type II errors in mapping quantitative trait loci. Genetics. 1994 Nov;138(3):871–881. doi: 10.1093/genetics/138.3.871. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jansen R. C. Interval mapping of multiple quantitative trait loci. Genetics. 1993 Sep;135(1):205–211. doi: 10.1093/genetics/135.1.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jansen R. C., Stam P. High resolution of quantitative traits into multiple loci via interval mapping. Genetics. 1994 Apr;136(4):1447–1455. doi: 10.1093/genetics/136.4.1447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kliman R. M., Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. doi: 10.1093/genetics/133.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lark K. G., Chase K., Adler F., Mansur L. M., Orf J. H. Interactions between quantitative trait loci in soybean in which trait variation at one locus is conditional upon a specific allele at another. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4656–4660. doi: 10.1073/pnas.92.10.4656. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laurie C. C., True J. R., Liu J., Mercer J. M. An introgression analysis of quantitative trait loci that contribute to a morphological difference between Drosophila simulans and D. mauritiana. Genetics. 1997 Feb;145(2):339–348. doi: 10.1093/genetics/145.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Long A. D., Mullaney S. L., Reid L. A., Fry J. D., Langley C. H., Mackay T. F. High resolution mapping of genetic factors affecting abdominal bristle number in Drosophila melanogaster. Genetics. 1995 Mar;139(3):1273–1291. doi: 10.1093/genetics/139.3.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Page R. E., Jr, Fondrk M. K., Hunt G. J., Guzmán-Novoa E., Humphries M. A., Nguyen K., Greene A. S. Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. J Hered. 2000 Nov-Dec;91(6):474–479. doi: 10.1093/jhered/91.6.474. [DOI] [PubMed] [Google Scholar]
- Van Ooijen JW LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity (Edinb) 1999 Nov;83(Pt 5):613–624. doi: 10.1038/sj.hdy.6886230. [DOI] [PubMed] [Google Scholar]
- Weber K., Eisman R., Higgins S., Morey L., Patty A., Tausek M., Zeng Z. B. An analysis of polygenes affecting wing shape on chromosome 2 in Drosophila melanogaster. Genetics. 2001 Nov;159(3):1045–1057. doi: 10.1093/genetics/159.3.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weber K., Eisman R., Morey L., Patty A., Sparks J., Tausek M., Zeng Z. B. An analysis of polygenes affecting wing shape on chromosome 3 in Drosophila melanogaster. Genetics. 1999 Oct;153(2):773–786. doi: 10.1093/genetics/153.2.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weinkove D., Neufeld T. P., Twardzik T., Waterfield M. D., Leevers S. J. Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor. Curr Biol. 1999 Sep 23;9(18):1019–1029. doi: 10.1016/s0960-9822(99)80450-3. [DOI] [PubMed] [Google Scholar]
- Wolf L. L., Starmer W. T., Polak M., Barker J. S. Genetic architecture of a wing size measure in Drosophila hibisci from two populations in eastern Australia. Heredity (Edinb) 2000 Dec;85(Pt 6):521–529. doi: 10.1046/j.1365-2540.2000.00763.x. [DOI] [PubMed] [Google Scholar]
- Yu S. B., Li J. X., Xu C. G., Tan Y. F., Gao Y. J., Li X. H., Zhang Q., Saghai Maroof M. A. Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9226–9231. doi: 10.1073/pnas.94.17.9226. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zeng Z. B. Precision mapping of quantitative trait loci. Genetics. 1994 Apr;136(4):1457–1468. doi: 10.1093/genetics/136.4.1457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zeng Z. B. Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):10972–10976. doi: 10.1073/pnas.90.23.10972. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zimmerman E., Palsson A., Gibson G. Quantitative trait loci affecting components of wing shape in Drosophila melanogaster. Genetics. 2000 Jun;155(2):671–683. doi: 10.1093/genetics/155.2.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zwaan B. J., Azevedo R. B., James A. C., Van 't Land J., Partridge L. Cellular basis of wing size variation in Drosophila melanogaster: a comparison of latitudinal clines on two continents. Heredity (Edinb) 2000 Mar;84(Pt 3):338–347. doi: 10.1046/j.1365-2540.2000.00677.x. [DOI] [PubMed] [Google Scholar]