THE EFFECTS OF INTERSPECIFIC COMPETITION ON THE DYNAMICS OF A POLYMORPHISM IN AN EXPERIMENTAL POPULATION OF DROSOPHZLA MELANOGASTER

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1 THE EFFECTS OF INTERSPECIFIC COMPETITION ON THE DYNAMICS OF A POLYMORPHISM IN AN EXPERIMENTAL POPULATION OF DROSOPHZLA MELANOGASTER ANDREW CLARK] Division of Bio-Medical Sciences, Brown Uniuersity, Providence, Rhode Island Manuscript received uly 21, 1978 Revised copy received December 22, 1978 ABSTRACT Populations of Drosophila melanogaster with a fourth-chromosome polymorphism were subjected to different levels of competition with Drosophila simulans. The dynamics of the polymorphism and the equilibrium frequencies of the sparkling allele were seen to depend on the competitive level, while the higher productivity of the competing populations was shown to be due to the initial parental density. The effects of competition on fitness components were quantified by fitting the data to both a two-stage selection model and a fertility model. Additional experiments were performed to verify that the interspecific competition caused the changes in fitness. The results are discussed in light of the importance of considering selection components in models of ecological genetics. Acentral problem in the study of population genetics is the measurement of genotypic fitness. In order to predict population dynamics, it is often insufficient to express fitness as a single parameter (PROUT 1965,1969). Several studies have demonstrated that more than one selection component can be implicated in the maintenance of polymorphisms (ALLARD and ADAMS 1969; BUNGAARD and CHRISTIANSEN 1972; CHRISTIANSEN and FRYDENBERG 197, 1976). CLDGG, KAHLER and ALLARD (1978) indicated, in addition, that selection may operate in different stages of the life cycle. It also appeared that differences in background genotype can change the apparent components of fitness at marker loci. The picture is made more complex by the fact that environmental variation may have different effects on different components of fitness. Many efforts have been made to quantify environmental factors that alter different components of fitness in Drosophila. BARKER (1971) and PARSONS (1975) presented studies on ecological differences between Drosophila species and the net effects of abiotic factors on fitness. The measurement of fitness of one gene was strongly influenced by variation in background genes. (ANDERSON 1969) and by the degree of polymorphism in a population (BEARDMORE et al. 1960). BIRCH (19555) presented a clear case of reversal of larval viabilities due to crowding, and WALLACE (197) showed that interspecific competitive ability depends on density. LEWONTIN and MATSUO (196) demonstrated that the fit- PreTent addiess Department of Biologcal Sciences, Stanford Umlersity, Stanford, California 905. Genetics 92: August, 1979

2 116 A. CLARK ness of an individual can depend on relative proportions of genotypes, and this phenomenon has also been observed in the form of rare-male mating advantage (EHRMAN 1966). Interspecific competition was chosen as the important environmental factor affecting fitness in this investigation, because competition is a central selective force in the theory of evolutionary ecology. The fact that genetic variation for competitive ability exists in Drosophila populations has been demonstrated by the response of this character to selection (MOORE 1952; AYALA 1969; FUTUYMA 1970; BARKER 197). The experiments of BARKER and PODGER (1970a, b) demonstrated that interspecific competition and increasing density in populations of D. melanogaster and D. simulans resulted in lower fecundity and larval viability, while other components of fitness remained relatively unaffected. Although they did not attempt to measure differences in fitness between genotypes within either species, they did demonstrate the complexity of the effects of interspecific competition, and they suggested that competition cannot be accurately measured by a single coefficient. The objective of this investigation was to determine whether different levels of interspecific competition could lead to changes in the genotypic fitness. MATERIALS AND METHODS To determine the effects of interspecific competition on fitness, the dynamics of a fourthchromosome polymorphism was observed in populations of D. melanogaster competing with D. simulans. Three levels of interspecific competition were employed with a total fly density of 150 in all populations at the beginning of each generation (Table 1). A laboratory stock of D. melanogaster with the fourth-chromosome balanced lethals, cp/i ()29, was crossed to sparkling poliert spaps1 homozygotes. The spapsl/l()29 genotypes were identified on the basis of their wild phenotype. The sparkling allele is recessive, and homozygotes appear to have fused eye facets. Homozygotes for 1()29 die in the egg stage. The frequency of crossing over in the fourth chromosome was very low and was ignored. All of the D. simulans were vermilion eye-color mutants, which made them easily distinguishable. Interspecific matings were found to occur at a negligible frequency. All of the D. melanogaster used to initiate the populations were spap61/1()29 in genotype, so that the initial allele frequency was 0.5. Note that throughout the experiment there were only two types of chromosome (one bearing the spnp61 allele, and the other bearing the lethal) so that the state of the polymorphism could be expressed in terms of either frequency. An 18-day discrete generation interval was maintained by observing the following procedure: Day 0-Populations were initiated at a sex ratio of 1:1 with 150 flies of the appropriate phenotypes and species (same age, virgin females). Day &Adults were removed from bottles, scored by phenotype, and discarded. Day 18-Adult progeny were removed and scored by phenotype. D. simulans progeny were discarded, and a sample of the D. melanogaster progeny was used to TABLE Experimental interspecific competitive levels: adult density at the start of each generation Population A B C D. melanogaster D. simulans

3 EFFECTS OF COMPE MTION ON FITNESS 117 initiate the next generation with genotypic frequencies identical to those among censused populations. D. simulans were added where appropriate from an outside stock to make the total fly density 150 at the start of each generation. A consequence of drawing D. simulans from an outside stock each generation is that they were not allowed to respond to selection for interspecific competitive ability, while the D. melanogaster populations could change in response to competition. To see if the fourth-chromosome polymorphism was important in the interspecific competitive ability of D. melanogaster, an auxiliary experiment was performed. Three replicate POPUlations were started with 50 spap6*/1()29 flies from the C populations after generation five of the main experiment, and 100 D. simulans from the common stock. Differences between these progeny counts and those of the C populations in the first generation of the main experiment indicate changes in D. melanogaster competitive ability independent of the sparkling allele frequency. A second auxiliary experiment was performed to separate the effects of D. melanogaster density and D. simulans competition. Three populations were started with 50, 100 and 150 virgin D. melanogrrster with a sparkling frequency of These adults were removed from the population bottles on the sixth day and the progeny were scored on day 18. Since D. simuluns were absent from these populations, any differences between them will be due to density effects independent of the specific competitive effects seen in the main experiment. This auxiliary experiment was replicated three times. The populations were raised in half-pint bottles on a standard cornmeal-molasses medium seeded with live yeast. All bottles were kept in a cycle of 12 hr of light and 12 hr of darkness at Four replicates of each competitive level in the main experiment were followed for six discrete generations. Fitness estimation Model I: An attempt was made to estimate relative fitnesses of the two viable D. melanogaster phenotypes by statistically fitting two models to the fourth-chromosome frequency data. The first model used is due to ANDERSON (1969). This model assumes that mating occurs at random, that selection operates independently of sex, and that fitness parameters are constant. The sparkling homozygote is assumed to have a fitness of one, and the estimates are of relative heterozygote fitness. The estimator is split into two temporal components. The early component (E) indicates the relative likelihood of survival from the zygote to the adult population sampling. The late component (L) represents the fitness from the sampling of the adults to the formation of zygotes, and thus includes adult mortality and fertility. By splitting the fitness into two components, the model avoids some of the problems associated with measuring fitness by a single parameter (PROUT 1965, 1969; CHRISTIANSEN and FRYDENBERG 197). The experimental design does not allow us to distinguish effects of zygotic, sexual, fecundity or gametic selection independently, but it does give a good approximation of net effects. ANDERSON S (1969 model describes the expected selectim dynamics by the relation: -= 1 (2 (L- (L-2-2W) (L-2-2W) Qt 0 w-1 )+ w-1 where q is the lethal alle frequency, and the net heterozygote fitness is W = E X L. If the heterozygote has a net fitness greater than the nonlethal homozygote (i.e. if W > I), a stable polymorphism will result with an equilibrium lethal allele frequency: (1) fj = (W-l)/(L-2--2W) (2) Maximum likelihood estimates of the fitness components were obtained with an iterative computer program, using FISHER S (1922) method. Model 2: Fertility differences are thought to play a major role in the evolution of Drosophila populations (see DISCUSSION). For this reason a model was designed that assumes selection to

4 ~ ~ A. CLARK TABLE 2 Model 2 fertility parameters.~ ~ Female AA Male Aa AA a P An P 1 occur as a result of differential mating success. The goodness-of-fit of the data to this model may give an indication f the importance of fertility differences in the context of this experiment. The model describes selection at a single diallelic locus, with one allele being lethal (sterile). It is a subset of the class of models described by HADELER and LIBERMAN (1975). Let the relative fertilities be as described in Table 2. If the frequencies of the genotypes AA and Aa are I-U and U, respectively, the resulting mating table is as shown in Table. Since there are only two alleles and two genotypes, and the model is sexually symmetric, it is one-dimensional. In particular, the recurrence relation for the frequency of heterozygotes is: But(l-ut) + %Vt2 Ut+l= -- a(l-~t)' + 2/~t(l-~t) + (0.75)~t' () The equation for the equilibrium heterozygote frequency is: S(a-2/+0.75) + i2(-2a+/-%) + V^(a-p) = 0 () The three roots are: ~ U" = 0, -- 2a--pS0.5 d/pz-a a-pfl.5 (5) A valid polymorphism will have O<v<2/ and will exist if: (Y 2 0, / 2 0, and (6) /' 2 (Y At most one polymorphic equilibrium can be stable, and the conditions for stability are: / > a, or (7) ff.b > I If the sexual symmetry is relaxed, so that mating AA x Aa has incidence P, and Aa X AA has incidence y. then all of the above relations hold with P replaced by the expression (B + Y)/2. TABLE Model 2 mating table giuing the outcomes of the matings in a single diallelic locus locus fertility model having a recessiue lethrrl allele Progeny XIating Mating success AA Aa aa. ~ AA X AA a(l-u)2 1 a 0 AA X Aa PU(1-U)?h?h 0 Aa XAA Pv (1 -U)?? 0 Aa XAa U2? '/z '/ (dies) U is the heterozygote frequency.

5 EFFECTS O F COMPETlTION ON FITNESS TABLE Competitive results 119 Generation B populations C populations 1.5% (1) 5.59% (58).79% (9) 6.% (71) O.W% (0) 1.87% (22) 0.00% (0) 0.62% (9) 0.29% (5) 0.17% () 0.00% (0) 0.55% (8) The first figure in each column represents the percentage of the progeny that were D. simdans, and the numbers in parentheses indicate the total counts of D. simulans. Note that D. mlanogaster had an apparent improvement in competitive ability as the experiment proceeded. Estimates of a and p were obtained by FISHER S (1992) method of maximum likelihood. The likelihood surfaces appeared to have a single maximum and convergence was rapid. RESULTS Competitive outcome D. simulans was at a competitive disadvantage relative to D. melanogaster in all populations. Furthermore, the relative proportion of D. simulans progeny declined over generations, suggesting a change in relative competitive abilities (Table ). The first auxiliary experiment demonstrated the relevance of the fourth chromosome polymorphism to the observed changes in competitive ability. After the fifth generation of the main experiment, three replicate populations were started with 50 ~pa*~~/1(,)29 flies from the C population, and 100 D. simulans from the common stock. In none of these populations were any D. simulans progeny observed, while 5.6% of the progeny of the main experiment first generation C populations were D. simulans. Since the sparkling frequency was the same (0.5) in both of these cases, and the competitive results were different, it would seem that the change in competitive ability is independent of the fourth chromosome polymorphism. It is possible that the apparent increase in D. melanogaster competitive ability was due to a decline in the competitive ability of D. simulans, but this seems very improbable. The D. simulans were drawn from an outside stock each generation, so that ability to compete with D. melanogaster was not subject to selection. The D. simulans stocks were kept under controlled laboratory conditions for 50 generations before the experiment began and were probably fairly stationary. Such a marked decrease in competitive ability in a single species stock in just six generations seems highly unlikely. The most probable explanation for the apparent increase in D. melanogaster competitive ability is theref ore genetic changes at loci other than those on the fourth chromosome. Polymorphism dynamics The lethal chromosome frequency had a familiar asymptotic trajectory in all populations (Figure 1, Table 5), and the polymorphic equilibria indicate a fit-

6 120 A. CLARK.5. > 0 z w 0 W. cc LL W w.2 a I t- w.i 0 I I I I I I 0 I G E NE R AT1 ON FIGURE 1.-Selection trajectories of the 1()29 lethal allele. Curves represent means over four replicates, and the bars represent f 2 standard errors. The A populations contained only D. melanogaster, while the B and C populations were subject to interspecific competition with D. simulans. ness advantage of the heterozygotes over the sparkling homozygotes. If all of the selection occurred before sampling each generation, then the frequency trajectory of the population with the smaller heterozygote advantage would always lie below a more strongly heterotic population. The occurrence of selection after sampling and before the formation of zygotes can result in an apparent non- constancy of fitness parameters (PROUT 1965, 1969). Thus, the crossing of the trajectories seen in Figure 1 does not necessarily indicate changes in relative fitness over time. One striking feature of the data is the similarity of the dynamics in the B and C populations, and their significant contrast to the A populations. An analysis of variance on angular transforms of the frequency data indicated that these differences were significant at a 5% level. The second auxiliary experiment was performed to see if these differences were due to competition with D. simulans _ or to different initial U. melanogaster densities. Populations started with 50, 100 and 150 virgin D. melanogaster with a sparkling frequency of 0.75 yielded progeny whose mean sparkling frequencies and standard errors were f 0.017, and 0.75 * 0.016, respectively. These means were not found to

7 EFFECTS OF COMPETITION ON FITNESS TABLE 5 Frequency of lethal-bearing chromosome among progeny scored on the 18th day oj each of six generations in four replicates and three levels of interspecific competition 121 A populations Generation Rep. 1 Rep. 2 Rep. Rep. Mean f S.E % f f t f f t 0.01 B populations I C ; 0.26 f f C populations t t f k t be significantly different, indicating that differences in initial D. melanogaster density does not necessarily cause changes in relative fitness. The differences between populations with and without D. simulans competition lead us to conclude that competition with D. simulans resulted in different relative fitnesses among genotypes in D. mezanogaster. This would be more convincing if there were no differences in sparkling allele frequency among progeny of different sized populations for any initial sparkling frequency. Productivity Large differences in productivity were observed between populations subjected to different levels of interspecific competition. It appeared that D. simu2ans improved the productivity of the D. melanogaster, because there were consistently more flies in mixed populations (Table 6). A nested analysis of variance was performed to test the statistical significance of this observation. The test revealed that at a 1 % level of significance the A populations had fewer progeny than the B and C populations, and the B and C populations were not different in productivity. The second auxiliary experiment attempted to distinguish between effects of D. simulans competition and D. melanogaster parental density. The means and standard errors of progeny densities of replicates, started with 50, 100 and 150 D. melanogaster, were , and , respectively. An analysis of variance indicated significant differences between these

8 122 A. CLARK TABLE 6 Densities of D. melanogaster adults scored on the 18th day of each of six generations in four replicates of three competitive levels A populations Generation Rep. 1 Rep. 2 Rep. Rep Mean 2 S.E f t f f f 28.9 B populations f f f f f 7.9 C populations f & f f f f treatments. The conclusion is that the different densities seen in the progeny of the different populations in the main experiment are probably due to different initial D. melanogaster densities, rather than to the effect of D. simulans competition. This is consistent with BARKER'S (197a) result, which indicated that there is an optimal adult density that maximizes productivity and that above this value the population productivity declines. The graph of mean adult productivities for different treatments over the six generations shows an increasing trend (Figure 2). This is consistent with the notion that the mean population fitness increases with the elimination of the lethal allele. A linear regression analysis was performed to test the statistical significance of the trend. Only the B populations had a significant regression coefficient (p < 0.025), indicating a mean increase in progeny density of flies per generation. The A and C populations had regression coefficients of 1.8 -C 7.0 and f 16.90, but these failed to have statistical significance. Fitness estimates Model I: Maximum likelihood estimates of the Anderson model fitness components are presented in Table 7. A single fitness estimate is obtained for each population which represents the best fit of equation (1) to the six generations of data. The expected frequency of heterozygotes for each generation and the x2 values for goodness-of-fit of the model to the data are also calculated. Note that, overall, the populations with interspecific competition do not fit the con-

9 EFFECTS OF COMPETITION ON FITNESS >. e 00 v) z W 0 >. Z W LL a I I I I I I 0 I GENERATION FIGURE 2.-D. melanogaster adult progeny density scored on the 18th day of each generation. Curves represent means over four replicates. Note the increasing trends and the lower productivity of the single species populations (curve A). stant-fitness model as well as do the single species populations. This may be due to a biotic interaction whose effect on fitness is regulated by phenotypic ratios. The populations came to an equilibrium gene frequency quite rapidly and stayed at a stationary value for the remaining generations. Estimating fitnesses on the basis of the trajectories thus places emphasis on the equilibrium allele frequencies. Once equilibrium is attained, additional information is not acquired by following the population for more generations (except to verify that it is in fact at an equilibrium), yet the x2 goodness-of-fit test increases in degrees of freedom. To test the importance of this observation, the fitness estimates were calculated together with their standard errors and the x2 values for the first four generations of data. These fitness estimates were not significantly different from the estimates based on all six generations of data. A x2 heterogeneity test was performed on the fitness estimates. It indicated that the populations were heterogeneous and that there was significant heterogeneity of fitness estimates between populations with different levels of competition. An analysis of variance was also performed on the fitness estimates to ascertain whether or not there were significant differences. This was legitimate be-

10 12 A. CLARK TABLE 7 Estimates of fitness components and their standard errors based on fits of the six generations of gene frequency data to ANDERSON S (1969) model A 1 populations 2 Replicate E C S.E. L C S.E f f f f f f 0.27 W f S.E. X 1.29 k f f f B 1 populations f f f t f k f f f f k f C 1 populations k f k f f k f f f k X20.O5() = 9.9 E, L and W represent the early, late and net fitnesses of the heterozygotes relative to the sparkling homozygotes. The x2 values represent goodness-of-fit of the model. cause the estimators are assumed to be independent and normally distributed. The mean fitnesses of the heterozygotes (W) relative to the homozygotes in populations A,B and C were 1.8,2.91 and 2.71, respectively. The statistical test indicated that the fitness of heterozygotes in the A populations was significantly lower than that of the other two, and the fitness values in the B and C populations were not significantly different ( p < 0.05). The higher heterozygote fitness in the competing populations resulted in a higher lethal allele frequency at equilibrium. Model 2: Since most of the fitness differences between the A, B, and C populations occurred in the L component, a fertility model was fit to the data (Table 8). The x2 values demonstrate even better fits of this model to the data than ANDER- SON S (1969) model, indicating that fitness in these populations is best thought of as a property of mating pairs rather than individual genotypes. If no viability selection had occurred, the expected frequency of sparkling among the progeny of the initial parents would be This frequency varies from 0.7 to 0.62 be- tween populations, but its mean value is The fact that the early fitness components in ANDERSON S model are fairly close to a value of 1.00 gives further credence to the notion that pre-sampling viability selection was not a major factor. The trend in the fertility model estimates seems to indicate an increase in heterogametic matings with increasing D. simulans competition. DISCUSSION Although the extent of competition was not quantified in this investigation,

11 EFFECTS OF COMPETITION ON FITNESS 125 TABLE 8 Model 2 fertility estimates and standard errors based on fits of the six generations of gene frequency data to the fertility model described in the text A 1 populations 2 Replicate (Y f S.E. fl 2 S.E. X= 0.76 t f f ) t t f k f B 1 populations 2 C 1 populations t f f t t f f f f f f f f k k f. 0. X20.O5() = 9.9,a and,g represent the relative mating success of AA X AA and AA x Aa matings, respectively. The x2 values represent goodness-of-fit of he model. its effect was clearly seen by the differences in trajectories between populations. If the degree of niche overlap is some indication of the degree of competition, then the two species studied would be expected to show strong competition. Being sibling species, D. melanogaster and D. simulans have very similar nutritional and SANG 1966; PARSONS 19751, and other niche components requirements (ERK are also similar. D. melanogaster can tolerate a broader range of temperature fluctuation (MILLER 196) and dessication (PARSONS 1975), but these factors should not have given D. melanogaster a strong competitive advantage in this experiment, since these parameters were held constant in the laboratory. Larval competition may have been reduced somewhat by the fact the D. simulans prefers to oviposit towards the center of the medium (BARKER 1971). The degree to which the two species are unable to coexist in the laboratory gives one indication of the significance of competition. A fundamental assumption of ANDERSON'S (1969) model is that fitness remains constant. Due to the fairly good fit of the data to this model, as indicated by the x2 values given in Table 5, this assumption appears reasonable. However, a single goodness-of-fit x2 value does not distinguish between a random scatter of points and a consistent deviation from the model. This failure to discriminate is especially evident when the data are examined graphically. Manipulation of equation (1) yields a linear relation between l/qt+l and l/qt with a slope of 1/W. Graphs of the data, however, show that the B and C populations are represented by monotonic curves rather than by a scatter of points about a straight line (Figure ). Since a steeper slope indicates a lower heterozygote fitness, it appears that the heterozygote fitness improves with time. Although fitnesses

12 126 A. CLARK W U a I t- W - I qt = (LETHAL ALLELE FREQUENCY AT TIME t I-' FIGURE.-Double reciprocal plot of the frequency of the lethal chromosome over successive generations. Curves are means over four replications. The diafonal line represents stable equilibria. apparently vary with genotype frequency. there is insufficient evidence to prove frequency dependent selection, because other factors also change as time proceeds. The ANDERSON (1969) fitness estimates seem to indicate that most of the differences between populations were due to fertility. This observation is strengthened somewhat by the goodness-of-fit of the strict fertility model to the data. The fact that the models fit the data well does not by itself imply that the assumptions of the models are correct. There is, however, no contradiction in the fact that the two different models fit the data presented here, since fertility is one component of ANDERSON'S (1969) model. Nevertheless, both models will not be able to fit all selection trajectories equally well. The fertility model may, for example, yield curved trajectories in the double reciprocal phase plot, as in Figure. Even though fertility parameters are constant, this apparent frequency dependence obtains because the mating probabilities vary with genotype frequencies. We are now in a position to ask why the heterozygotes have improved fitness when they are competing with D. simulans. There are experimental results to indicate that differential mating behavior may account for the increased heterozygote fitness. CONNOLLY, BURNET and SEWELL (1969) demonstrated that eye pigmentation is an important component of courtship behavior in D. melangaster and suggested that it may be a factor in mating success. GREER and GREEN

13 EFFECTS OF COMPETITION ON FITNESS 127 [ 1962), working with the multi-allelic white-eye locus, found that differential mating success and degree of eye pigmentation were strongly correlated. RAs- MUSON and LUNG (197) also found evidence that differential mating success due to eye pigmentation maintained a deleterious gene in polymorphism. In their detailed study of selection components, BUNGAARD and CHRISTIANSEN (1972) showed that the spapoz allele was maintained in a polymorphism due to differential mating success, while zygotic, gametic and fecundity selection had little importance. Although proof of the mechanism was not presented here, it would seem that the presence of D. stmulans differentially affected the mating success of the two phenotypes of D. melanogaster. This observation is consistent with the results of both models that were fit to the data. The implication is that models of density dependence (e.g., ANDERSON 1971 ; ROUGHGARDEN 19711, frequency dependence (AYALA and CAMPBELL 197; DEBENEDICTIS 1977) and interspecific competition should be extended to include effects of these environmental factors on fertility. I thank M. T. CLECG and. F. KIDWELL for their guidance, and M. W. FELDMAN and T. PROUT for their suggestions and stimulating discussion. I also thank W. W. ANDERSON for use of his fitness estimating program. LITERATURE CITED ALLARD, R. W. and. ADAMS, 1969 Population studies in predominantly self-pollinating species XIII. Intergenotypic competition and population structure in barley and wheat. Am. Naturalist 10: ANDERSON, W. W., 1969 Selection in experimental populations I. Lethal genes. Genetics 62: , 1971 Genetic equilibrium and population growth under density regulated selection. Am. Naturalist 105: AYALA, F.., 1969 Evolution of fitness IV. Genetic evolution of interspecific competitive ability in Drosophila. Genetics 61 : AYALA, F.. and C. A. CAMPBELL, 197 Frequency dependent selection. Ann. Rev. Ecol. Syst. 5: BARKER,. S. F., 1971 Ecological differences and competitive interactions between D. melanogaster and D. simulans in small laboratory populations. Oecologia 8: , 197a Adult population density. fecundity and productivity in D. melanogaster. Oecologia 11: , 197b Natural selection for coexistence or competitive ability in laboratory populations of Drosophila. Egypt.. Genet. Cytol. 2: BARKER,. S. F. and R. N. PODGER, 1970a Interspecific competition between D. mehogaster and D. simulans: effects of larval density on viability, developmental period and adult weight. Ecology 51: , 197Ob Interspecific competition between D. melanogaster and D. simulans: effects of larval density and short term adult starvation on fecundity, egg hatchability, and adult viability. Ecology 51 : 855-8W. BEARDMORE,. M., TH. DoszHa~sx~ and 0. A. PAVLOVSKY, 1960 An attempt to compare the the fitness of polymorphic and monomorphic experimental populations of D. melanogaster. Heredity 1: 19-. BIRCH, L. C., Selection in D. pseudwbscura in relation to crowding. Evolution 9: 89- BUNGAARD,. and F. B. CHRISTIANSEN, 1972 Dynamics of polymorphisms: I. Selection components in an experimental population of D. melanogaster. Genetics 71 : 9-60.

14 128 A. CLARK CHRISTIANSEN, F. B. and 0. FRYDENBERG, 197 Selection component analysis of natural polymorphisms using population samples including mother-child combinations. Theoret. Pop. Biol. : , 1976 Selection component analysis of natural polymorphisms using mother-offspring samples of successive cohorts. pp. --. In: Population Genetics and Ecology, Edited by S. KARLIN and E. NEVO, Academic Press, New York. CLEGG, M. T., A. L. KAHLER and R. W. ALLARD, 1978 Estimation of life cycle components of selection in an experimental plant population. Genetics 8: CONNOLLY, R., B. BURNET and D. SEWELL, 1969 Selective mating and eye pigmentation: an analysis of the visual component in the courtship behavior of D. melanogaster. Ecology 2 : DEBENEDICTIS, P. A., 1977 Studies in the dynamics of genetically variable populations I. Frequency anud density dependent selection in experimental populations of Drosophila Genetics 87: -56. EHRMAN, L., 1966 Mating success and genotype frequency in Drosophila. Anim. Behav. 1: 2-9. Em, F. C. and. H. SANG, 1966 The comparative nutritional requirements of two sibliing species D. simulans and D. melanogaster.. Insect Physiol. 12: -51. FISHER, R. A., 1922 On the dominance ration. Proc. Soc. Edinb. Sect. B 2: 99-. FUTUYMA, D.., 1970 Variation in genetic response to interspecific competition in laboratory populations of Drosophila. Am. Naturalist 10 : GREER, B. W. and M. M. GREEN, 1962 Genotype, phenotype and mating behavior of D. melanogaster. Am. Naturalist 96: HADELER, K. P. and U. LIBERMAN, 1975 Selection models with fertility differences.. Math. Biol. 2: LEWONTIN, R. and Y. MATSUO, 196 Interaction of genotypes determining viability in D. buskii. Proc. Natl. Acad. Sci. U.S. 9: MANNING, A., 1959 The sexual isolation between D. melanogaster and D. simulans. Anim. Behav. 7: MILLER, R. S., 196 Larval competition between D. melanogaster and D. simulans. Ecology 5: MOORE,. A., 1952 Competition between D. melanogaster and D. simulans 11. The improve. ment of competitive ability through selection. Proc. Natl. Acad. Sci. U.S. 8: PARSONS, P. A., 1975 The comparative evolutionary biology of the sibling species D. melanogaster and D. simulans. Quart. Rev. Biol. 50: PROUT, T., 1965 The estimation of fitness from genotypic frequencies. Evolution 19: , 1969 The estimation of fitness from population data. Genetics 6: RASMUSON, M. and A. LUNG, 197 Fitness and fitness components for a two allele system in D. melanogaster. Hereditas 7: ROUGHGARDEN,., 1971 WALLACE, B., Density dependent natural selection. Ecology 52: Studies on intra- and interspecific competition in Drosophila. Ecology 55: Corresponding editor: R. W. ALLARD