Copyright 0 1994 by the Genetics Society of America Linearity Versus Nonlinearity of Offspring-Parent Regression:An Experimental Study of Drosophila melanogaster A. Gimelfarb and J. H. Willis Department of Biology, University of Oregon, Eugene, Oregon 97403 Manuscript received November 20, 1993 Accepted for publication June 9, 1994 ABSTRACT An experiment was conducted to investigate the offspring-parent regressionfor three quantitative traits (weight, abdominal bristles and wing length) in Drosophila melanogaster. Linear and polynomial models were fitted for the regressions of a character in offspringon both parents. It is demonstrated that responses by the characters to selection predicted by the nonlinear regressions may differ substantiallyfrom those predicted by the linear regressions. This is true even, and especially, if selection is weak. The realized heritability for a character under selection is shown to be determined not only by the offspring-parent regression but also by the distribution of the character and by the form and strength of selection. HE following well known formula of quantitative with the wing tip and the anteriorcrossvein. KELLER and T genetics is customarily used to predict theresponse MITCHELL(1962) found no evidence of either domi- to selection by a quantitative trait: nance or epistasis for the wing length (they measured the distance from the humeral plate at the base of the = h2S, (1) R wing to its tip). where R is the response, S is the selection differential The following notations for the traits will be used in and h2 is the narrow sense heritability. Implicit in this the paper: WTD and WTS for weight of daughters and formula is the assumption that the offspring-parent re- sons, BD and BS for the numberof bristleson daughters gression is linear. Thisassumption is rarely questioned. and on sons, WGD and WGS for the wing length in Yet, FRANKHAM(1990) has compiled data illustrating the daughters and in sons. asymmetry ofresponses to directional selection on com- ponents of reproductive fitness indicating apossibility of MATERIALS AND METHODS nonlinearity in the offspring-parent regression for such The data on the weight and abdominal bristles were col- traits. It has also been demonstrated theoretically that lected from a base population originated from a stock pro- dominance of allelic effects (BULMER1985; GIMELFARB vided to us by BRIANCHARLESWORTH. The population was main- tained in 10 bottles (approximately 150 flies per bottle) with 1986a) or skewness in the distribution of the environ- a mixing every two weeks of adult flies between the bottles as mental component (NISHIDAand ABE 1974) can cause a described by ROSE and CHARLESWORTH(1981). A batch of 10 nonlinearity in the regression. There are,undoubtedly, families was initiated by collecting 20 virgin females and 20 other hereditary and developmental mechanisms that males (grandparents) from the base population and mating can render the offspring-parent regression nonlinear. them randomly (one pair in a vial). On the 14th day after mating, 10 virgin females and 10 males (onlyone fly from each The purpose of the current study was to investigate vial) were collectedand kept separately. At the age of two days directly the linearity (or nonlinearity) of the offspring- these twenty flies (parents) were weighed, their bristles were parent regression for a number of quantitative traits in scored, and they were randomly mated(one pair in a vial). On Drosophila melanogaster, and to see how nonlinearities, the 14th day after mating, two virgin offspring of each sex were if found, affect our inferences about responses by the collected from each vial. Like their parents, they were kept separately, and their weight and bristle scorewere obtained on characters to selection. The following three traits were the second day of their life. The total of 22 batches were es- involved in the study: tablished, out of which 176 families with complete data have Weight (in milligrams). For this trait, KF,ARSEY and been recovered. The complete data for a family included KOJIMA(1967) have presented evidence ofweak epistasis. weights and bristle scoresof the mother, the father, two sisters and two brothers. No special effort was made tocontrol for the Abdominal bristles (on segments 4 and 5 in females density other than always removing parents from a vial on the and onsegments 3 and 4 in males). KELLER and MITCHELL 8th day and collecting offspring on the 14th day. All batches (1962) found evidence of weakdominance andepistasis were maintained at 24( ?l)O. Collections were made using for this trait. CLAWONet al. (1957) attributed 9% of the CO,, whereas for weighing and bristle scoring the flies were total phenotypic variance by the abdominal bristles in a etherized. laboratory population to “genetic complexities.” The data on the wing length of parents and their offspring (two sisters and two brothers) in 159 families were given to us Wing length(in millimeters) measured as the distance by JERRY COYNE.They come from the experiment 3 (parents between the intersections of the third longitudina1 vein and offspring reared in the laboratory) reported by COWEand Genetics 138: 343-352 (October, 1994) 344 andA. Gimelfarb J. H. Willis TABLE 1 Parameters of parental and offspring distributions ~~~ Weight (mg) Bristles Wing (mm) Mean SD Mean SD Mean SD Mothers0.112 1.202 3.92 45.18 0.058 1.540 Daughters0.127 1.075 2.87 45.21 0.056 1.514 Fathers0.075 0.862 3.35 38.06 1.354 0.046 Sons 0.813 0.068 37.83 0.0442.74 1.355 BEECHAM(1987), and these authorscan be consulted for the is not significant (P = 0.3). There is a significant dif- description of the data and experimental procedures. ference (P<0.05) between the regressions of daughters Table 1 shows the mean and standard deviation for the char- acters under consideration. Thereis a significant difference in and of sons for all traits. the mean of each character between sexes. A significant dif- As has been mentioned earlier, thecoefficient of lin- ference existsalso between parents and offspring in their ear regression of offspring on the mid-parental value is mean weight: the offspring weigh less, on the average, than used as an estimate of the heritability defined as the ratio parents of the same sex. This can beattributed to the fact that of the additive component of variance to the total phe- theparental parents (grandparents) were notexposed to ether, whereas the offspring’s parents were etherized twicein notypic variance. If a character is standardized, this co- order to weigh themand score their bristles.It has been dem- efficient is equal to the sum of the coefficients in (3). onstrated by GIMELFAREIand WILLIS(1988) that exposing flies Hence, for thestandardized characters discussed in the to ether reduces theweight of their offspring.Also, the mean paper theheritability estimated by the regression on the wing length in daughters and mothers differ significantly,but mid-parental value is an explanation for this is not known. The offspring-parent regressions were fitted separately for h2 = b, + b/. (4) daughters and for sons. The charactersof the two sibs of the same sex were averaged so that an “offspring character” ina The estimated heritabilities are shown in Table 2. Also regression is in fact the arithmetic average of the character shown in the table are thecoefficients of determination, among the two sibs. Also, all characters (in parents as well as R2.This parameter measures the proportion of the vari- in offspring) were standardized prior to fittinga regression by subtracting the mean and dividing over the standard deviation.ance among the offspring explainable by thecorre- Hence, each character ina regression has zero mean andunit sponding regression on parents. The higher R2is, the variance. Statistical analyses were performed using the soft- more accurate prediction about the character in off- ware SYSTAT (WILKINSON1990) on a PC 486 computer. spring can be made based on the charactersof parents. Nonlinear offspring-parent regressions RESULTS AND DISCUSSION Linear offspring-parent regressions Before fitting nonlinear regressions we have excluded observations that were outliers in the linearregressions The coefficient of linear regression of the offspring’s (the coefficients reported in Table 3 are, in fact, with the character on the characterof onlyone of the parentsor outliers left out). An observation was considered anout- on the mid-parental value is often used to estimate the lier if the actual value of the characterdiffered by more narrow sense heritability and, consequently, to predict than 2.5 SD from the value predicted by the regression. the response by the character toselection based on for- It is usually recommended in text books on linear re- mula (1).In reality, though, theresponse is determined gression to check for outliers as a possible indication of by the regression on the charactersin both parents.For the nonlinearity in the regression. We have decided, this reason, we fitted the regression however, to be conservative and tomake sure that a non- linearity, if found, is not due to just few outliers but is, f(x,y) = x, yl (2) indeed, a “solid” nonlinearity. Therefore, the nonlin- of the character in offspring, z, on the character of the earities that we have found probably underestimate the mother, x, and of the father, y. Table 2 shows the CO- nonlinearities in the actual offspring-parent regressions efficients of linear regression, for the characters under consideration. In the three-dimensional space, the linear regression f(x, y) = b,x + by, (3) function f(x,y) in (3) represents a plane. There are fitted to the family data for all of the characters. There many different biological mechanisms that can make is no constant term in the regression function since the the offspring-parent regression nonlinear so that the characters in parents and in offspring arestandardized.