Fitness of allozyme variants in Drosophila pseudoobscura III. Possible factors contributing to the maintenance of polymorphisms in nature

Experiments have been performed to investigate the mechanisms maintaining enzyme polymorphisms in natural populations. We have measured effects on fitness of genotypic variants at three loci, Est-5, Odh, and Mdh-2, in D. pseudoobscura. Significant differences exist among the genotypes in the rate of development from egg-to-adult; there is also indication of differences in larval survival. In a population segregating for allelic variants at all three loci, there is indication that segregation distortion at meiosis or some form of gametic selection might be involved. The relative fitnesses of alternative genotypes are reversed when either different fitness components are considered, or the genotypic frequencies are changed, or the larval density is increased. These fitness reversals may contribute to the maintenance of the polymorphisms, and may account for cyclical oscillations of allozyme frequencies observed in natural populations.Research supported by U.S. Public Health Service Research Fellowship (1F05 TWO 1991-01) to D.M. and by contract AT(04-3)34 with the U.S. Atomic Energy Commission. Adress reprint requests from Europe to D.M.; from elsewhere to F.J.A.     

The Experimental Assessment of Fitness in Drosophila. II. a Comparison of Competitive and Noncompetitive Measures

Twelve diverse strains of Drosophila melanogaster have been examined with respect to their individual fitness components and with respect to their relative performance under competitive and noncompetitive conditions. Individual fitness components included estimates of time until successful copulation (t), fecundity (f) and egg-to-adult viability (v), and a composite index of overall fitness of the form fv/t was used for comparisons among strains. Noncompetitive performance was assessed in terms of the biomass (standing crop) and productivity of equilibrium experimental populations. Competitive performance was assessed in terms of relative competitive ability vis-à-vis a standard compound-autosome-bearing strain in single-generation tests. A significant correlation was found between the composite index of individual fitness components and the competitive compound-autosome test. Although the biomass and productivity of equilibrium populations were correlated with each other, neither of these noncompetitive measures was correlated with individual fitness components or with the composite index. We suggest that the performance of strains in such noncompetitive tests may be related to what Wright has called the "mean selective value" of the populations. Judging from their association with the composite index of individual fitness components, competitive tests such as the compound-autosome test seem to be related more nearly to the average Darwinian fitness of the populations.     

Minimizing kinship in captive breeding programs

Captive populations of endangered species are managed to preserve genetic diversity and retain reproductive fitness. Minimizing kinship (MK) has been predicted to maximize the retention of gene diversity in pedigreed populations with unequal founder representation. MK was compared with maximum avoidance of inbreeding (MAI) and random choice of parents (RAND) using Drosophila melanogaster. Forty replicate populations of each treatment were initiated with unequal founder representation and managed for four generations. MK retained significantly more gene diversity and allelic diversity based on six microsatellite loci and seven allozyme loci than MAI or RAND. Reproductive fitness under both benign and competitive conditions did not differ significantly among treatments. Of the methods considered, MK is currently the best available for the genetic management of captive populations. Zoo Biol 16:377–389, 1997. © 1997 Wiley-Liss, Inc.     

The effect of lead on fitness components and developmental stability in Drosophila subobscura

We analyzed the developmental time, egg-to-adult viability, and developmental stability (fluctuating wing size asymmetry) in Drosophila subobscura, maintained for six generations on different concentrations of lead. Development time is significantly affected by generation and lead concentration, but interaction of these factors is not a significant source of variability for this fitness component. Generation and the interaction generation x concentration of lead significantly affect egg-to-adult viability. Levene's test of heterogeneity of variance showed that variability of FA is not significant in any of the samples. Within both lead concentrations females showed significantly higher FA indices for the wing width than males. Within sexes, a significantly higher FA was found only in females for wing width FA between the control and the lower concentration of lead. The results show that if strong relationship between FA and the studied fitness components exists, it results in a stronger selection of unstable genotypes under lead as a stress factor and, consequently, FA needs to be used with caution as a biomarker in natural populations under environmental stress.     

Allozyme diversity among local populations of the pacific mussel <Emphasis Type="Italic">Mytilus trossulus</Emphasis> (Bivalvia: Mytilidae) from polluted areas of Peter the Great Bay (Sea of Japan)

Allozyme variability was assessed, using starch gel electrophoresis, at 15 polymorphic loci in two samples of the Pacific mussel Mytilus trossulus collected from local populations in heavily (Golden Horn Bay) and slightly polluted areas (Sukhoputnaya Bay) of Peter the Great Bay. Significant differences between samples were found in the genotypic frequencies at nine loci and in allele frequencies, at six loci. The results are suggestive of the differential survival of individuals having different genotypes and alleles at some of the surveyed loci under conditions of pollution. Our data are not in conflict with the hypothesis of the adaptive significance of allozyme polymorphism.     

Frequency-Dependent Selection at the LAP Locus in DROSOPHILA MELANOGASTER

Results of fitness estimates for the Lap locus in Drosophila melanogaster revealed that under crowded media conditions gene frequency equilibrium was maintained by frequency-dependent selection. Evidence was obtained that indicated that mating and egg-to-adult viability were frequency dependent.     

Growing with siblings: a common ground for cooperation or for fiercer competition among plants?

Recent work has shown that certain plants can identify their kin in competitive settings through root recognition, and react by decreasing root growth when competing with relatives. Although this may be a necessary step in kin selection, no clear associated improvement in individual or group fitness has been reported to qualify as such. We designed an experiment to address whether genetic relatedness between neighbouring plants affects individual or group fitness in artificial populations. Seeds of Lupinus angustifolius were sown in groups of siblings, groups of different genotypes from the same population and groups of genotypes from different populations. Both plants surrounded by siblings and by genotypes from the same population had lower individual fitness and produced fewer flowers and less vegetative biomass as a group. We conclude that genetic relatedness entails decreased individual and group fitness in L. angustifolius. This, together with earlier work, precludes the generalization that kin recognition may act as a widespread, major microevolutionary mechanism in plants.     

Density- and Frequency-Dependent Selection at the Mdh-2 Locus in DROSOPHILA PSEUDOOBSCURA

We have studied differences in the number of Drosophila pseudoobscura produced in a culture when the flies differ with respect to two alleles (F and S) at the Mdh-2 locus, which codes for a malate dehydrogenase enzyme. The studies were done at low and at high density in two- and three-genotype combinations (S/S, F/F and S/F), with one-genotype cultures as controls.——Density affects the fitness of the Mdh-2 genotypes. Different genotypes are differently affected, and the genotype of the competitors also makes a difference on the fitness of a given genotype. When three genotypes are present in a culture, particularly at high density, intergenotypic competition is less intense than intragenotypic competition at several frequency combinations. That is, there is "overcompensation": the three genotypes together exploit the environmental resources better than one genotype alone.—The fitness of the genotypes is frequency dependent in both two-genotype and three-genotype combinations. An inverse relationship between frequency and fitness is observed at high density. This may lead to a stable polymorphism, because the fitness of a genotype increases as its frequency decreases.—Forty independent strains, sampled from a natural population, were used in the experiments. This ensures that more than 95% of the variation present in the genome in the natural population is also present is the experimental cultures. It also ensures that the genetic background of the Mdh-2 alleles is randomized in the same way as it is in nature. However, the possibility remains that Mdh-2 alleles in nature are nonrandomly associated with alleles at closely linked loci. If linkage disequilibrium is present in the experiments because it exists in nature, then the observed effects (such as frequency-dependent selection) would affect the Mdh-2 locus in nature as well.     

Genetic features of root fungus-resistant scotch pine trees in artificial stands in the steppe zone of Ukraine

A comparative analysis of the allozyme variation in 18 loci of three steppe natural populations of Pinus sylvestris L. and a sample of 36 resistant trees from artificial stands at locations affected by root fungus (Heterobasidion annosum (Fr.) Bref.) is conducted. The resistant trees are characterized by lowest percentages of polymorphic allozyme loci, a fewer number of alleles, and number of genotypes close to the mean-population number, as well as a level of observed and expected heterogeny. In terms of composition and frequencies of multi-loci genotypes (Dia-1, Lap-1, Acp) that are responsible for the greatest contribution to the partitioning of the stands studied, the sample of resistant trees differs markedly from the natural populations.     

A MULTILEVEL APPROACH TO THE SIGNIFICANCE OF GENETIC VARIATION IN ALCOHOL DEHYDROGENASE OF DROSOPHILA

Prior studies showed that differences in alcohol dehydrogenase (ADH) activity across genotypes of Drosophila are decisive for the outcome of selection by ethanol. In the present paper, the effect on ADH activity and egg-to-adult survival of combinations of ethanol, propan-2-ol, and acetone in naturally occurring concentrations is examined. Propan-2-ol is converted into acetone by ADH in vitro. Acetone is considered a competitive inhibitor of ethanol for the ADH enzymes. The melanogaster-ADH-S allozyme is two times more sensitive towards inhibition by acetone than either simulans-ADH or melanogaster-ADH-F. The physiological implications of these in vitro differences for larvae were studied in short-term in vivo and long-term exposure experiments. No major differences in acetone accumulation or fitness parameters were found between the strains in response to ecologically relevant concentrations of acetone or propan-2-ol. Ethanol, however, strongly decreased egg-to-pupal survival in both Drosophila simulans strains and increased developmental time in four out of the five strains tested. Therefore, under physiological conditions only ethanol was shown to act as a selective agent on the ADH polymorphism during egg-to-pupa development in Drosophila.     

Genetic Background and the Fitness of Allozymes

Experimental perturbations of gene frequency at the esterase-5 locus in Drosophila pseudoobscura were carried out in a series of population cages started with differing numbers of founder chromosomes. Cages founded with few chromosomes showed changes in gene frequency at the allozyme locus. Such changes were less marked in cages founded with a larger sample of chromosomes. These experiments show the importance of linkage disequilibrium in affecting allozyme frequencies, and emphasize the necessity of careful experimental design when studying fitness differences between allozymes in laboratory populations.     

Population genetics of Drosophila amylase. V. Genetic background and selection on different carbohydrates

Frequency changes in amylase allozymes and patterns of tissue-specific expression of amylase have been monitored in laboratory populations of Drosophila pseudoobscura maintained on media in which the only carbohydrate source was maltose or starch. Nonrandom changes occurred in patterns of expression, whereas no patterns in allozyme frequency changes were discernible. The nature of the pattern changes was similar to an identical study done on populations derived from a natural population several hundred miles from the population used in the present experiments. However, in the previous study nonrandom changes in allozyme frequencies were also noted. Evidently, selection on the Drosophila amylase system differs depending upon the genetic background of the population. Furthermore, the evolutionary dynamics of structural gene variants and those regions controlling its expression may be independent, a result consistent with DNA sequence data.     

Competitive fitness in experimental populations of Drosophila willistoni

Experiments are reported in which genetically different strains of Drosophila willistoni compete with D. pseudoobscura. The competition was studied at three temperatures, 20°, 22°, and 25°C. The outcome of the competition depends on the genetic constitution of the competing species, but at 25° and 22°C D. willistoni flies are generally stronger competitors than D. pseudoobscura, while at 20°C D. pseudoobscura generally has a competitive advantage. There is a significant interaction between genotype and temperature; the strain RP3 is the weakest competitor of all D. willistoni strains at 22° and 25°C, but not at 20°C; the strain M18 is the best competitor at 20° and 22°C but not at 25°C.The performance of the four strains of D. willistoni was measured in two more ways. First we estimated their Darwinian fitness relative to other genotypes of the same species. Second, we measured the average population size of each strain in pure culture. There is no significant correlation between population size in pure culture and either competitive fitness or Darwinian fitness. There is, however, a strong positive correlation between Darwinian fitness and interspecific competitive fitness.It is pointed out that natural selection leads to an increase in the average Darwinian fitness of a population but not necessarily to an increase in its adaptedness to the environment. Yet the synthetic theory of evolution assumes that the genes and genotypes favored by natural selection are usually those which increase the adaptedness of their carriers to the environments where they live. The correlation between Darwinian fitness and adaptedness needs to be studied experimentally.This work was supported by NSF grant GB-12562 (International Biological Program), AEC contract AT-(30-1)-3096, and PHS Career Development Award K3GM 37265 to F. J. Ayala. The senior author's stay in New York was financed in part by Research Fellowship 2-12861 from the Panamerican Union.     

The Alcohol Dehydrogenase Polymorphism in Populations of DROSOPHILA MELANOGASTER. I. Selection in Different Environments

The allozyme polymorphism at the alcohol dehydrogenase locus in Drosophila melanogaster was studied in order to obtain experimental evidence about the maintenance of this polymorphism. Populations started with different initial allele frequencies from homozygous F and S lines showed a convergence of frequencies on regular food at 25 degrees, leading to values equal to those in the base populations. These results were interpreted as due to some kind of balancing selection. In populations kept at 29.8 degrees, a lower equilibrium F frequency was attained. Addition of ethanol and some other alcohols to the food gave a rapid increase in F frequency, and high humidity decreased the F frequency slightly. Combination or alternation of ethanol and high humidity had variable effects in the populations tested. For a further analysis of the allele-frequency changes, estimates were obtained for egg-to-adult survival under different conditions and for adult survival on ethanol-supplemented food. On ethanol food (both at regular and high humidity), egg-to-adult survival of SS homozygotes was considerably lower than that of the FF and FS genotypes. Under regular conditions of food, temperature and humidity, a tendency to heterozygote superiority was observed, while at high humidity a relative high survival of SS was noticed in some tests. Adult survival of SS was lower than that of FF, but FS was generally intermediate, though the degree of dominance differed between populations. The results are consistent with the hypothesis of the occurrence of selection at the Adh locus.     

Fitness of wild‐caught Drosophila melanogaster females: allozyme variants of GPDH, ADH, PGM, and EST

We have collected several hundred Drosophila melanogaster flies (near Davis, California), isolated them individually, without anesthesia, at the collecting site, and estimated the fitness components of the wild‐caught females under different environmental conditions. The fitness parameters measured are fecundity, oviposition rate, and productivity (egg‐to‐adult viability, development rate, and number of progeny). The environmental variables are two temperatures (22°C and 28°C) and two densities (‘scant’ and ‘crowded’). After the fitness measurements are completed for each individual female, its genotype is determined at four loci encoding enzymes: GPDH and ADH, located on chromosome II and PGM and EST‐C, located on chromosome III. Density has a large significant effect on productivity; temperature has significant effects on fecundity, oviposition rate, and development rate. The experiments show that allozyme polymorphisms are associated with selection effects. Fitness differences between allozyme genotypes occur for all fitness components, except oviposition rate. But which genotype is superior depends on the environmental conditions; heterozygotes exhibit higher fitness than homozygotes in a number of cases, but inferior in others. A unique feature of the present experiments is that the experimental flies are wild‐caught females rather than laboratory‐bred individuals. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genic heterozygosity, chromosomal interchanges and fitness in rye: any relationship?

Relationship between heterozygosity at allozyme loci, chromosomal interchanges and fitness was analyzed in a rye cultivar showing a polymorphism for such rearrangements. Nine allozyme systems (ACO, ACPH, GOT, GPI, LAP, MDH, PER, PGD and PGM) and five components of fitness (number of fertile tillers, total offspring, egg cell fertility, flowers/ear and seeds/ear) were studied. The estimated selection coefficients against interchange heterozygotes ranged from s = 0.12 to s = 0.34. A significant effect of the genic heterozygosity on some fitness components was observed in interchange heterozygotes (tillering and total offspring), in their standard homozygous sibs (flowers/ear and seeds/ear) and in the descendants of the crosses between standard karyotypes (flowers/ear, seeds/ear and egg cell fertility). However, the main effect was linked to genetic background associated to different crosses. Significant differences for Acph-1, Gpi-1, Lap-1, Mdh-1, Mdh-4, Pgd-2 and Pgm-1 loci were also found in some of these crosses although these differences were inconsistent. This suggests that probably the allozyme loci analyzed were not directly contributing to the fitness and that they are linked, in some cases, to different deleterious alleles depending on both cross and locus. This fact could support the local effect hypothesis as explanation although we do not discard the existence of some inbreeding level (general effect hypothesis) since all crosses and loci studied show a overall consistent trend of increased fitness with increased heterozygosity.     

Enzyme Variability in Natural Populations of DAPHNIA MAGNA III. Genotypic Frequencies in Intermittent Populations

In temporary habitats populations of the cyclical parthenogen, Daphnia magna, are re-established each year from sexual eggs and reproduce parthenogenetically for two or at most three generations. The genetic effects of this breeding system have been investigated by analyzing allozyme frequencies in nineteen intermittent populations.—Genotypic frequencies at polymorphic loci were ordinarily found to be in good agreement with Hardy-Weinberg proportions and disequilibria between loci were not observed. Although significant changes in gene frequencies were observed both during and between successive cycles, there was no evidence of the marked instability of genotype frequencies characteristic of permanent populations. The recombinational degradation of genotypes at the end of each annual cycle in temporary habitats effectively prevents the genotypic structuring which develops when continued parthenogenesis is possible.     

A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. I. Estimates of Gene Flow from Rare Alleles

In order to assess the evolutionary significance of molecular variation in natural populations of Drosophila melanogaster, we have started a comprehensive genetic variation study program employing a relatively large number of gene-protein loci and an array of populations obtained from various geographic locations throughout the world. In this first report we provide estimates of gene flow based on the spatial distributions of rare alleles at 117 gene loci in 15 worldwide populations of D. melanogaster . Estimates of Nm (number of migrants exchanged per generation among populations) range from 1.09 in East-Asian populations (Taiwan, Vietnam and Australia) to 2.66 in West-Coast populations of North America. These estimates, among geographic populations separated by hundreds or even thousands of miles, suggest that gene flow among neighboring populations of D. melanogaster is quite extensive. This means that, for selectively neutral genes, we should expect little differentiation among neighboring populations. A survey of eight West-Coast populations of D. melanogaster (geographically comparable to Drosophila pseudoobscura) showed that in spite of extensive gene flow, populations of D. melanogaster show much more geographic differentiation than comparable populations of D. pseudoobscura. From this we conclude that migration in combination with natural selection rather than migration alone is responsible for the geographic uniformity of molecular polymorphisms in D. pseudoobscura.     

Direct Evidence of Genic Differentiation between Sex Ratio and Standard Gene Arrangements of X Chromosome in DROSOPHILA PSEUDOOBSCURA

Evidence of strong association of alleles at the Esterase-5 and adult Acid phosphatase-6 loci with the Sex Ratio and the Standard X chromosome arrangements in D. pseudoobscura is presented. There is no differentiation at these two loci, either in the Sex Ratio or the Standard arrangement from two widely separated geographic populations. At the Esterase-5 locus, alleles characteristic of one arrangement are found in low frequencies in the other arrangement. It is concluded, from these and other observations that the differentiation between the Sex Ratio and the Standard arrangement, at these two loci, is a result of natural selection favoring different coadapted gene blocks in these arrangements. The average heterozygosity at these two loci in different karyotypes is in the following order: ST/SR > ST/ST >> SR/SR which agrees very well with the fitness estimates of these karyotypes.     

Naturally segregating loci exhibit epistasis for fitness

The extent to which gene interaction or epistasis contributes to fitness variation within populations remains poorly understood, despite its importance to a myriad of evolutionary questions. Here, we report a multi-year field study estimating fitness of Mimulus guttatus genetic lines in which pairs of naturally segregating loci exist in an otherwise uniform background. An allele at QTL x5b—a locus originally mapped for its effect on flower size—positively affects survival if combined with one genotype at quantitative trait locus x10a (aa) but has negative effects when combined with the other genotypes (Aa and AA). The viability differences between genotypes parallel phenotypic differences for the time and node at which a plant flowers. Viability is negatively correlated with fecundity across genotypes, indicating antagonistic pleiotropy for fitness components. This trade-off reduces the genetic variance for total fitness relative to the individual fitness components and thus may serve to maintain variation. Additionally, we find that the effects of each locus and their interaction often vary with the environment.