Spontaneous Mutational Variances and Covariances for Fitness-Related Traits in Drosophila melanogaster

Abstract Starting from a completely homozygous population of Drosophila melanogaster, 176 lines were derived and independently maintained by a single brother-sister mating per generation. Three fitness-related traits were considered (fecundity, egg-to-pupa and pupa-to-adult viabilities). Mutational heritabilities of these traits and genetic correlations between all possible pairs were calculated from the between line divergence (codivergence), after 104–106 generations of mutation accumulation. Mutational heritabilities ranged from 0.60 × to 0.82 × 10−3 and correlations from −0.11 to 0.25. These values are likely to be underestimates due to selection against deleterious mutations. The distribution of the means of the lines was asymmetric, positive for fecundity and negative for both viability components. The coefficients of asymmetry are also likely to be biased, again due to selection. Extreme lines from the two tails of the distribution were examined in detail. Homozygous line effects were all negative for viability traits but predominantly positive for fecundity, indicating the fixation of mutations with positive effects on the latter. Corresponding heterozygous line effects showed a variable degree of dominance.

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The Rate of Mutation and the Homozygous and Heterozygous Mutational Effects for Competitive Viability: A Long-Term Experiment With Drosophila melanogaster

Genetics ◽

10.1093/genetics/158.2.681 ◽

2001 ◽

Vol 158 (2) ◽

pp. 681-693 ◽

Cited By ~ 7

Author(s):

David Chavarrías ◽

Carlos López-Fanjul ◽

Aurora García-Dorado

Keyword(s):

Drosophila Melanogaster ◽

Minimum Distance ◽

Deleterious Mutations ◽

Regression Estimate ◽

Term Experiment ◽

Degree Of Dominance ◽

Long Term Experiment ◽

Rate Of Decline ◽

Good Agreement

Abstract The effect of 250 generations of mutation accumulation (MA) on the second chromosome competitive viability of Drosophila melanogaster was analyzed both in homozygous and heterozygous conditions. We used full-sib MA lines, where selection hampers the accumulation of severely deleterious mutations but is ineffective against mildly deleterious ones. A large control population was simultaneously evaluated. Competitive viability scores, unaffected by the expression of mutations in heterozygosis, were obtained relative to a Cy/L2 genotype. The rate of decline in mean ΔM ≈ 0.1% was small. However, that of increase in variance ΔV ≈ 0.08 × 10-3 was similar to the values obtained in previous experiments when severely deleterious mutations were excluded. The corresponding estimates of the mutation rate λ ≥ 0.01 and the average effect of mutations E(s) ≤ 0.08 are in good agreement with Bateman-Mukai and minimum distance estimates for noncompetitive viability obtained from the same MA lines after 105 generations. Thus, competitive and noncompetitive viability show similar mutational properties. The regression estimate of the degree of dominance for mild-to-moderate deleterious mutations was ∼0.3, suggesting that the pertinent value for new unselected mutations should be somewhat smaller.

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The genetic structure of natural populations of Drosophila melanogaster. XXIV. Effects of hybrid dysgenesis on the components of genetic variance of variability.

Genetics ◽

10.1093/genetics/127.3.545 ◽

1991 ◽

Vol 127 (3) ◽

pp. 545-552

Author(s):

D S Suh ◽

T Mukai

Keyword(s):

Drosophila Melanogaster ◽

Population Genetic ◽

Genetic Parameters ◽

Genetic Variance ◽

Additive Genetic Variance ◽

Natural Populations ◽

Deleterious Mutations ◽

Degree Of Dominance ◽

Population Genetic Parameters ◽

P Type

Abstract Eight hundred second chromosomes were extracted from the Ishigakijima population, one of the southernmost populations of Drosophila melanogaster in Japan. Half of them were extracted in Native cytoplasm (P-type), and half in Foreign cytoplasm (M-type). Various population-genetic parameters, including the frequency of lethal-carrying second chromosomes (Q = 0.235 for the Native; 0.218 for the Foreign), the allelism rate of lethal second chromosome (Ic = 0.0217 for the Native; 0.0134 for the Foreign), the homozygous detrimental and lethal loads (D = 0.179 for the Native; 0.270 for the Foreign; L = 0.262 for the Native; 0.240 for the Foreign), the average degree of dominance of mildly deleterious mutations (ĥE = 0.244 for the Native; 0.208 for the Foreign), and the components of genetic variance for viability [additive (sigma A2) and dominance (sigma D2)](ŝigma A2 = 0.0187 for the Native; 0.0172 for the Foreign; ŝigma D2 = 0.0005 for the Native; 0.0009 for the Foreign) were estimated. The data indicate that D was significantly larger and hE was significantly smaller in the Foreign cytoplasm. However, the estimates of additive and dominance variances were not significantly different between the two cytoplasms. The additive genetic variance for viability in the Ishigakijima population was greater than expected on the basis of mutation-selection balance confirming previous studies on papers of D. melanogaster in warm climates.

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Age-Specific Patterns of Genetic Variance in Drosophila melanogaster. II. Fecundity and Its Genetic Covariance With Age-Specific Mortality

Genetics ◽

10.1093/genetics/143.2.849 ◽

1996 ◽

Vol 143 (2) ◽

pp. 849-858 ◽

Cited By ~ 5

Author(s):

Marc Tatar ◽

Daniel E L Promislow ◽

Aziz A Khazaeli ◽

James W Curtsinger

Keyword(s):

Drosophila Melanogaster ◽

Variance Components ◽

Life History Traits ◽

Genetic Variance ◽

Additive Genetic Variance ◽

Genetic Correlations ◽

Mutation Accumulation ◽

Age Classes ◽

Genetic Covariance ◽

Specific Mortality

Abstract Under the mutation accumulation model of senescence, it was predicted that the additive genetic variance (VA) for fitness traits will increase with age. We measured age-specific mortality and fecundity from 65,134 Drosophila melanogaster and estimated genetic variance components, based on reciprocal crosses of extracted second chromosome lines. Elsewhere we report the results for mortality. Here, for fecundity, we report a bimodal pattern for VA with peaks at 3 days and at 17–31 days. Under the antagonistic pleiotropy model of senescence, it was predicted that negative correlations will exist between early and late life history traits. For fecundity itself we find positive genetic correlations among age classes >3 days but negative nonsignificant correlations between fecundity at 3 days and at older age classes. For fecundity vs. age-specific mortality, we find positive fitness correlations (negative genetic correlations) among the traits at all ages >3 days but a negative fitness correlation between fecundity at 3 days and mortality at the oldest ages (positive genetic correlations). For age-specific mortality itself we find overwhelmingly positive genetic correlations among all age classes. The data suggest that mutation accumulation may be a major source of standing genetic variance for senescence.

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On the Rate and Linearity of Viability Declines in Drosophila Mutation-Accumulation Experiments: Genomic Mutation Rates and Synergistic Epistasis Revisited

Genetics ◽

10.1093/genetics/166.2.797 ◽

2004 ◽

Vol 166 (2) ◽

pp. 797-806 ◽

Cited By ~ 4

Author(s):

James D Fry

Keyword(s):

Mutation Rate ◽

Average Rate ◽

Natural Populations ◽

Mutation Accumulation ◽

High Rate ◽

Deleterious Mutations ◽

Order Of Magnitude ◽

Contamination Event ◽

Genomic Mutation ◽

The 1960S

Abstract High rates of deleterious mutations could severely reduce the fitness of populations, even endangering their persistence; these effects would be mitigated if mutations synergize each others’ effects. An experiment by Mukai in the 1960s gave evidence that in Drosophila melanogaster, viability-depressing mutations occur at the surprisingly high rate of around one per zygote and that the mutations interact synergistically. A later experiment by Ohnishi seemed to support the high mutation rate, but gave no evidence for synergistic epistasis. Both of these studies, however, were flawed by the lack of suitable controls for assessing viability declines of the mutation-accumulation (MA) lines. By comparing homozygous viability of the MA lines to simultaneously estimated heterozygous viability and using estimates of the dominance of mutations in the experiments, I estimate the viability declines relative to an appropriate control. This approach yields two unexpected conclusions. First, in Ohnishi’s experiment as well as in Mukai’s, MA lines showed faster-than-linear declines in viability, indicative of synergistic epistasis. Second, while Mukai’s estimate of the genomic mutation rate is supported, that from Ohnishi’s experiment is an order of magnitude lower. The different results of the experiments most likely resulted from differences in the starting genotypes; even within Mukai’s experiment, a subset of MA lines, which I argue probably resulted from a contamination event, showed much slower viability declines than did the majority of lines. Because different genotypes may show very different mutational behavior, only studies using many founding genotypes can determine the average rate and distribution of effects of mutations relevant to natural populations.

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Supergene degeneration opposes polymorphism: The curious case of balanced lethals

10.1101/2021.11.27.470204 ◽

2021 ◽

Author(s):

Emma Berdan ◽

Alexandre Blanckaert ◽

Roger K Butlin ◽

Thomas Flatt ◽

Tanja Slotte ◽

...

Keyword(s):

Equilibrium State ◽

Balancing Selection ◽

Mutation Accumulation ◽

Small Population ◽

Quasi Equilibrium ◽

Deleterious Mutations ◽

Critical Factors ◽

Critical Aspect ◽

Allopatric Divergence

Supergenes offer some of the most spectacular examples of long-term balancing selection in nature but their origin and maintenance remain a mystery. A critical aspect of supergenes is reduced recombination between arrangements. Reduced recombination protects adaptive multi-trait phenotypes, but can also lead to degeneration through mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes. One such outcome is the formation of balanced lethal systems, a maladaptive system where both supergene arrangements have accumulated deleterious mutations to the extent that both homozygotes are inviable, leaving only heterozygotes to reproduce. Here, we perform a simulation study to understand the conditions under which these different outcomes occur, assuming a scenario of introgression after allopatric divergence. We found that AOD aids the invasion of a new supergene arrangement and the establishment of a polymorphism. However, this polymorphism is easily destabilized by further mutation accumulation. While degradation may strengthen AOD, thereby stabilizing the supergene polymorphism, it is often asymmetric, which is the key disrupter of the quasi-equilibrium state of the polymorphism. Furthermore, mechanisms that accelerate degeneration also tend to amplify asymmetric mutation accumulation between the supergene arrangements and vice versa. As the evolution of a balanced lethal system requires symmetric degradation of both arrangements, this leaves highly restricted conditions under which such a system could evolve. We show that small population size and low dominance coefficients are critical factors, as these reduce the efficacy of selection. The dichotomy between the persistence of a polymorphism and degradation of supergene arrangements likely underlies the rarity of balanced lethal systems in nature.

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THE ALCOHOL DEHYDROGENASE POLYMORPHISM IN POPULATIONS OF DROSOPHILA MELANOGASTER. I. SELECTION IN DIFFERENT ENVIRONMENTS

Genetics ◽

10.1093/genetics/90.1.161 ◽

1978 ◽

Vol 90 (1) ◽

pp. 161-191

Author(s):

W van Delden ◽

A C Boerema ◽

A Kamping

Keyword(s):

Drosophila Melanogaster ◽

Alcohol Dehydrogenase ◽

Experimental Evidence ◽

Balancing Selection ◽

Adult Survival ◽

High Survival ◽

High Humidity ◽

Allozyme Polymorphism ◽

Degree Of Dominance ◽

Frequency Changes

ABSTRACT 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°, 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°, 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.

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A quantitative genetic study of starvation resistance at different geographic scales in natural populations of Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672310000327 ◽

2010 ◽

Vol 92 (4) ◽

pp. 253-259 ◽

Cited By ~ 12

Author(s):

JULIETA GOENAGA ◽

JUAN JOSÉ FANARA ◽

ESTEBAN HASSON

Keyword(s):

Drosophila Melanogaster ◽

Genetic Correlations ◽

Natural Populations ◽

Food Shortage ◽

Population Variation ◽

Phenotypic Variance ◽

Starvation Resistance ◽

Natural Genetic Variation ◽

Quantitative Genetic ◽

Variation Explained

SummaryFood shortage is a stress factor that commonly affects organisms in nature. Resistance to food shortage or starvation resistance (SR) is a complex quantitative trait with direct implications on fitness. However, surveys of natural genetic variation in SR at different geographic scales are scarce. Here, we have measured variation in SR in sets of lines derived from nine natural populations of Drosophila melanogaster collected in western Argentina. Our study shows that within population variation explained a larger proportion of overall phenotypic variance (80%) than among populations (7·2%). We also noticed that an important fraction of variation was sex-specific. Overall females were more resistant to starvation than males; however, the magnitude of the sexual dimorphism (SD) in SR varied among lines and explained a significant fraction of phenotypic variance in all populations. Estimates of cross-sex genetic correlations suggest that the genetic architecture of SR is only partially shared between sexes in the populations examined, thus, facilitating further evolution of the SD.

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Quantitative Genetics of Drosophila Melanogaster. II. Heritabilities and Genetic Correlations between Sexes for Head and Thorax Traits.

Genetics ◽

10.1093/genetics/119.2.421 ◽

1988 ◽

Vol 119 (2) ◽

pp. 421-433

Author(s):

D E Cowley ◽

W R Atchley

Keyword(s):

Drosophila Melanogaster ◽

Sexual Dimorphism ◽

Genetic Analysis ◽

X Chromosome ◽

Dosage Compensation ◽

Imaginal Disc ◽

Genetic Correlations ◽

Body Parts ◽

Quantitative Genetic ◽

Males And Females

Abstract A quantitative genetic analysis is reported for traits on the head and thorax of adult fruit flies, Drosophila melanogaster. Females are larger than males, and the magnitude of sexual dimorphism is similar for traits derived from the same imaginal disc, but the level of sexual dimorphism varies widely across discs. The greatest difference between males and females occurs for the dimensions of the sclerotized mouthparts of the proboscis. Most of the traits studied are highly heritable with heritabilities ranging from 0.26 to 0.84 for males and 0.27 to 0.81 for females. In general, heritabilities are slightly higher for males, possibly reflecting the effect of dosage compensation on X-linked variance. The X chromosome contributes substantially to variance for many of these traits, and including results reported elsewhere, the variance for over two-thirds of the traits studied includes X-linked variance. The genetic correlations between sexes for the same trait are generally high and close to unity. Coupled with the small differences in the traits between sexes for heritabilities and phenotypic variances, these results suggest that selection would be very slow to change the level of sexual dimorphism in size of various body parts.

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