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An Introgression Analysis of Quantitative Trait Loci That Contribute to a Morphological Difference Between Drosophila Simulans and D

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An Introgression Analysis of Quantitative Trait Loci That Contribute to a Morphological Difference Between Drosophila Simulans and D Copyight 0 1997 by the Genetics Societv of America An Introgression Analysis of Quantitative Trait Loci That Contribute to a Morphological Difference Between Drosophila simulans and D. mauritiana Cathy C. Laurie, John R. True, Jianjun Liu and John M. Mercer Department of Zoology, Duke University, Durham, North Carolina 27708 Manuscript received August 12, 1996 Accepted for publication October 29, 1996 ABSTRACT Drosophila simulans and D. maum'tiana differ markedly in morphology of the posterior lobe, a male- specific genitalic structure. Bothsize and shapeof the lobe can be quantifiedby a morphometric variable, PC1, derived from principal components and Fourier analyses. The genetic architectureof the species difference in PC1 was investigated previously by composite interval mapping, which revealed largely additive inheritance, with a minimum of eight quantitative trait loci (QTL) affecting the trait. This analysis was extended by introgression of marked segments of the maun'tiana third chromosome into a simulans background by repeated backcrossing. Thetwo types of experiment are consistentin suggesting that several QTL on the third chromosome may have effects in the range of 10-15% of the parental difference andthat all or nearly all QTL have effects in the same direction. Since the parental difference is large (30.4 environmental standard deviations), effects of this magnitude can produce alternative homozygotes with little overlap in phenotype. However, these estimates may not reflect the effects of individual loci, since each interval or introgressed segment may contain multiple QTL. The consistent direction of allelic effects suggests a history of directional selection on the posterior lobe. HE genetic analysis of a quantitative trait usually ual genes that affect continuously variable traits. The T begins with a pair of strains that differ widely in new tools are of two types. One type consists of experi- the value of the trait. These strains are intercrossed to mental techniques for the detection and convenient produce segregating populations, which then are ana- assay of molecular marker variation, which allows local- lyzed to estimate the number,locations and distribution ization of QTL due to cosegregation in F2 or backcross of effects of the quantitative trait loci (QTL) that con- populations (reviewed by TANKSLEY1993). The second tribute to the parental difference. The results of this type of tool consists of statisticaltechniques forinterval analysis may provide inferences about the evolutionary mapping, which utilize molecular marker data to local- processes that caused the trait difference between the ize and estimate the effects of QTL (LANDER and pair of strains being analyzed and possibly about the BOTSTEIN1989; ZENC 1994 and others). genetic structure of their common ancestral popula- The new QTL techniques have been utilized exten- tion. For example, analysis of a cultivated plant and its sively to analyze cultivated plants and their wild relatives wild ancestor may reveal the types of genetic variants (TANKSLEY1993), with interesting implications for crop that were utilized during the historical process of do- evolution under domestication (e.g., DOEBLEYet al. mestication. In contrast,analysis of pairs of natural spe- 1995). However, so far therehave been only a few inter- cies may provide information about thetypes ofgenetic val mapping studies motivated by an interest in natural variants that become fixed under natural (rather than populations. For example, LONGet al. (1995) have ana- artificial) selection, operating over long time periods. lyzed high and low bristle number lines of Drosophila, Analysis of divergent lines produced by short-term arti- produced by short-term artificial selection, to make in- ficial selection may reveal information about standing ferences about standing variation in a base population. variation in the base population, whereas such informa- In addition, BRADSHAWet al. (1995) have analyzedfloral tion may be obscured in theanalysis of population pairs differences between Mimulus species to understand the that have been isolated for long periodsof time. Thus, genetic basis of isolating mechanisms. each situation potentially provides novel types of infor- We have initiated a detailed genetic analysis of a dif- mation about quantitative trait evolution. ference in male genital morphology between species of In recent years there has been a resurgence of inter- Drosophila (LIUet al. 1996).Two closelyrelated species, est in quantitative trait evolution because of the devel- D. simulans and D. mauritiana, differ markedly in the size and shape of the posterior lobe of the genital arch opment of new tools for detectingand mapping individ- (Figure 1). This morphological difference can be quan- tified by a morphometric descriptor (PC1) based on Corresponding author: Cathy C. Laurie, DCMB/Zoology, Box 91000, Duke University, Durham, NC 27708. elliptical Fourier and principal components analyses. E-mail: [email protected] Previously, the genetic architecture of this trait was in- Genetics 145 999-348 (Frbrnay, 1997) 840 C. C. Laurie el (IC. FIGURE1.-The ventral portion of the genital arch from D. simulnns and D. mauritiuna. The lateral plate is covered with bristles, while the posterior lobe has only a single bristle at its base. D. simulans D. mauritiana vestigated by hybridizing inbred lines of each species to in flies to be used for morphological analysis. Control produce two backcross populations of -200 individuals introgressions were also performed by repeated back- each, which were analyzedjointly by composite interval crossing of the mauritiana host strain (without P ele- mapping (ZENG 1994) with the aid of 18 marker loci. ments) to assess the effects of any residual maun'tianu The parental lines showed a large difference in PC1 material that is not associated with the selected P ele- (30.4 environmental SD) and the markers accounted ment. Thedifference in posterior lobe morphology be- for >80% of the phenotypic variation. Among 15 inter- tween the P-marked introgression lines and the controls vals analyzed, eight showed convincing evidence of gives information about the magnitude of QTL effects. QTL, and the range of estimated QTL effects was 5.7- This information provides a useful comparison with es- 15.9% of the parental difference. Although there was timates from interval mapping, which is based on a very some evidence for partial dominance of maun'tiana al- different methodology. In addition, the introgression leles and for epistasis, the pattern of inheritance of PC1 lines allow a direct visualization of the effects of small is largely additive. chromosomal segments on posterior lobe morphology. Here we extend our previous study of posterior lobe morphology by supplementingthe interval mapping re- MATERIALSAND METHODS sults with an introgression analysis. The focus of this Drosophila stocks: The experiment was initiated with a ana1ysis is the third chromosome^ which appears to 'On- 7uhi/p mutant stock of each species, both provided by J. A. tain the greatest nw~~berof QTL, as well as those QTL COYNE.From the initially outbred simulnns 7u stock ( 18w), an with the largest effects. The basic approach is to intro- inbred line (13wI) was derived by 20 generations of full sib gress marked segments of the maun'tiana third chromo- mating and subsequently maintained by mass transfer. AIl crosses were carried out on standard cornmeal-molasses me- SOme into a simulans genetic background. A total of 48 dium at room temperature. positions throughoutthe chromosome were tagged Construction and cytogenetic analysis of mauritiana stocks with a P-dement insertion containing a selectable eye Gth Rw+]insem The mari'liana 7u stock was transformed color marker (Figure 2). Each maun'liann insert stock, by embryo injection with a Pelement containinga mini-white which contains a single Pelement, was hybridized and gene, 13Lac-70+1 (BIER d a[. 1989), to produce a set of single- then backcrossed for 15-24 generations to a simulans insert transformant stocks. These insertions are stable because of lack of endogenous Pelements.Each Pinsert was localized strain, producing a set Of marked introgression lines* by in silu hybriclization to the polytene chromosomes(Figure Then the Pekment (and associated maudianachromo- 2) and the recombination fraction between pairs of inserts at soma1 segment) in each line was made homozygous adjacent locations was estimated toproduce a genetic map. :wv vvv VWT" v :I: v v vvvw w wwv v vv v vv vv v f v 61 162 163 lU k5 1% 167 168 169 170 b1172b3 b4h5 b6 b7 h8 b91.&183 1841 931 921 911 901 891 881 871 861 851{)94 195 1% 197 198 199 I I I\ Id0 80 81 3rd chromosome FIGURE2.-Cytogenetic locations of the p[ru'] insertions introduced into a w mutant strain of D. mnuritiana. A total of 48 third chromosome insertions at 42 distinct locations are represented. Thejagged lines in 3R represent a fixed inversion difference between D.mnuritiana and D. melanogastpr; otherwise, those two species have homosequential polytene chromosomes (LEMEUNIER and ASHBURNER 1976). Introgression Xn;dysis in DrosopI1ila 3-1 1 D.nmuririona mating schcmc~samples a single introgrcwerl segtnct1t from D. simslons H' - one male pel- srthline and makes it homozygotts in thc malrs P[loc-w+l insertion- V that \vu"' rrsctl for nlorphological analysis (csccpt for cross- overs that occur in fc~tnalcsduring thc 1;~cross). D..simulons D m,t,t,iwta A total of 21 I~;~ckcrosscontrol srrhlinrs ~vet-calso cotl- -/X =& strrtctcd by using the same introgrcssion proccrlurc. csccp that thrl-r was no I' clcnlcnt in thc vwuri/i/rj//tliw that \\':IS FI lhyhrd crossed to .xiwtt/urr.s in thr first generation and, thct-cfixc.110 R-/x =dY cyc color markrr to selcct each gcncration. ~\tnongtllcse RE!!% x BdY 21 suhlincs, 11 went tht-ough tllc s;ltnc mating schemr and I maintcnancc rcgimc ;IS the fisctl sul~lincs;Ind IO u~nt repealedbackcrossing I for 15 generations I through thr samc rcgimc ;IS thc nonfisctl sublines. I Sampling males for morphological analysis: Two s(*ts of I lines wcrc sntnplcdat tlifli~renttimcs to obtain males for Inor- J.
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