scholarly journals A non-coding indel polymorphism in the fruitless gene of Drosophila melanogaster exhibits antagonistically pleiotropic fitness effects

2021 ◽  
Vol 288 (1950) ◽  
Author(s):  
Michael D. Jardine ◽  
Filip Ruzicka ◽  
Charlotte Diffley ◽  
Kevin Fowler ◽  
Max Reuter
Keyword(s):  
Drosophila Melanogaster ◽  
Genetic Variation ◽  
Balancing Selection ◽  
Antagonistic Pleiotropy ◽  
Multiple Target ◽  
Indel Polymorphism ◽  
Fitness Components ◽  
Fitness Effects ◽  
Males And Females ◽  
Opposing Effects

The amount of genetic variation for fitness within populations tends to exceed that expected under mutation–selection–drift balance. Several mechanisms have been proposed to actively maintain polymorphism and account for this discrepancy, including antagonistic pleiotropy (AP), where allelic variants have opposing effects on different components of fitness. Here, we identify a non-coding indel polymorphism in the fruitless gene of Drosophila melanogaster and measure survival and reproductive components of fitness in males and females of replicate lines carrying each respective allele. Expressing the fruitless region in a hemizygous state reveals a pattern of AP, with one allele generating greater reproductive fitness and the other conferring greater survival to adulthood. Different fitness effects were observed in an alternative genetic background, which may reflect dominance reversal and/or epistasis. Our findings link sequence-level variation at a single locus with complex effects on a range of fitness components, thus helping to explain the maintenance of genetic variation for fitness. Transcription factors, such as fruitless , may be prime candidates for targets of balancing selection since they interact with multiple target loci and their associated phenotypic effects.

scholarly journals A non-coding indel polymorphism in the fruitless gene of Drosophila melanogaster exhibits antagonistically pleiotropic fitness effects

2020 ◽  
Author(s):  
Michael D. Jardine ◽  
Filip Ruzicka ◽  
Charlotte Diffley ◽  
Kevin Fowler ◽  
Max Reuter
Keyword(s):  
Drosophila Melanogaster ◽  
Genetic Variation ◽  
Balancing Selection ◽  
The Other ◽  
Antagonistic Pleiotropy ◽  
Indel Polymorphism ◽  
Fitness Components ◽  
Fitness Effects ◽  
Males And Females ◽  
Opposing Effects

AbstractThe amount of genetic variation for fitness within populations tends to exceed that expected under mutation-selection-drift balance. Several mechanisms have been proposed to actively maintain polymorphism and account for this discrepancy, including antagonistic pleiotropy (AP), where allelic variants have opposing effects on different components of fitness. Here we identify a non-coding indel polymorphism in the fruitless gene of Drosophila melanogaster and measure survival and reproductive components of fitness in males and females of replicate lines carrying one or the other allele. Expressing the fruitless region in a hemizygous state we observe a pattern of AP, with one allele resulting in greater reproductive fitness while the other confers greater survival to adulthood. Different fitness effects were observed in an alternative genetic background, suggesting widespread epistatic effects. Our findings link sequence-level variation at a single locus with complex effects on a range of fitness components, thus helping to explain the maintenance of genetic variation for fitness. Transcription factors, such as fruitless, may be prime candidates for targets of balancing selection since they interact with multiple target loci and their associated phenotypic effects.

scholarly journals Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster

2014 ◽  
Vol 281 (1788) ◽  
pp. 20140987 ◽  
Author(s):  
Crystal M. Vincent ◽  
Nathaniel P. Sharp
Keyword(s):  
Drosophila Melanogaster ◽  
Genetic Variation ◽  
Sexual Dimorphism ◽  
Bacterial Pathogen ◽  
Ecological Factors ◽  
Evolutionary Genetics ◽  
Antagonistic Pleiotropy ◽  
Sexual Antagonism ◽  
Heritable Variation ◽  
Dioecious Populations

A critical task in evolutionary genetics is to explain the persistence of heritable variation in fitness-related traits such as immunity. Ecological factors can maintain genetic variation in immunity, but less is known about the role of other factors, such as antagonistic pleiotropy, on immunity. Sexually dimorphic immunity—with females often being more immune-competent—may maintain variation in immunity in dioecious populations. Most eco-immunological studies assess host resistance to parasites rather than the host's ability to maintain fitness during infection (tolerance). Distinguishing between resistance and tolerance is important as they are thought to have markedly different evolutionary and epidemiological outcomes. Few studies have investigated tolerance in animals, and the extent of sexual dimorphism in tolerance is unknown. Using males and females from 50 Drosophila melanogaster genotypes, we investigated possible sources of genetic variation for immunity by assessing both resistance and tolerance to the common bacterial pathogen Pseudomonas aeruginosa. We found evidence of sexual dimorphism and sexual antagonism for resistance and tolerance, and a trade-off between the two traits. Our findings suggest that antagonistic pleiotropy may be a major contributor to variation in immunity, with implications for host–parasite coevolution.

scholarly journals Causes of natural variation in fitness: Evidence from studies of Drosophila populations

2015 ◽  
Vol 112 (6) ◽  
pp. 1662-1669 ◽  
Author(s):  
Brian Charlesworth
Keyword(s):  
Population Genetics ◽  
Genetic Variation ◽  
Balancing Selection ◽  
Large Contribution ◽  
Deleterious Mutations ◽  
Weak Selection ◽  
Fitness Components ◽  
Genetic Studies ◽  
Standing Variation ◽  
Available Information

DNA sequencing has revealed high levels of variability within most species. Statistical methods based on population genetics theory have been applied to the resulting data and suggest that most mutations affecting functionally important sequences are deleterious but subject to very weak selection. Quantitative genetic studies have provided information on the extent of genetic variation within populations in traits related to fitness and the rate at which variability in these traits arises by mutation. This paper attempts to combine the available information from applications of the two approaches to populations of the fruitfly Drosophila in order to estimate some important parameters of genetic variation, using a simple population genetics model of mutational effects on fitness components. Analyses based on this model suggest the existence of a class of mutations with much larger fitness effects than those inferred from sequence variability and that contribute most of the standing variation in fitness within a population caused by the input of mildly deleterious mutations. However, deleterious mutations explain only part of this standing variation, and other processes such as balancing selection appear to make a large contribution to genetic variation in fitness components in Drosophila.

scholarly journals Self-fertilization and inbreeding limit the scope for sexual antagonism

2014 ◽  
Author(s):  
Samuel J. Tazzyman ◽  
Jessica K. Abbott
Keyword(s):  
Genetic Variation ◽  
A Priori ◽  
Interactive Effect ◽  
Natural Populations ◽  
Sexual Antagonism ◽  
Considerable Evidence ◽  
Fitness Effects ◽  
Genomic Location ◽  
Self Fertilization ◽  
Males And Females

Sexual antagonism occurs when there is a positive intersexual genetic correlation in trait expression but opposite fitness effects of the trait(s) in males and females. As such, it constrains the evolution of sexual dimorphism and may therefore have implications for adaptive evolution. There is currently considerable evidence for the existence of sexually antagonistic genetic variation in laboratory and natural populations, but how sexual antagonism interacts with other evolutionary phenomena is still poorly understood in many cases. Here we explore how self-fertilization and inbreeding affect the maintenance of polymorphism for sexually antagonistic loci. We expected a priori that selfing should reduce the region of polymorphism, since inbreeding reduces the frequency of heterozygotes and speeds fixation. Although this expectation was supported, our results show that there is an interactive effect between the degree of selfing and dominance such that those segregating sexually antagonistic loci that do exist are more likely to be partially dominant. In addition, inbreeding effects may influence population persistence and genomic location of sexually antagonistic loci in separate-sexed organisms.

scholarly journals FITNESS EFFECTS OF EMS-INDUCED MUTATIONS ON THE X CHROMOSOME OF DROSOPHILA MELANOGASTER. I. VIABILITY EFFECTS AND HETEROZYGOUS FITNESS EFFECTS

Genetics ◽  
1977 ◽  
Vol 87 (4) ◽  
pp. 763-774
Author(s):  
Joyce A Mitchell
Keyword(s):  
Drosophila Melanogaster ◽  
X Chromosome ◽  
Strongly Correlated ◽  
Induced Mutations ◽  
X Chromosomes ◽  
Heterozygous Condition ◽  
Fitness Effects ◽  
Sucrose Solutions ◽  
Discrete Generation ◽  
Males And Females

ABSTRACT Drosophila melanogaster X chromosomes were mutagenized by feeding males sucrose solutions containing ethyl methanesulfonate (EMS); the concentrations of EMS in the food were 2.5 mm, 5.0 mm, and 10.0 mm. Chromosomes were exposed to the mutagen up to three times by treating males in succeeding generations. After treatment, the effective exposures were 2.5, 5.0, 7.5, 10.0, 15.0, and 30.0 mm EMS. X chromosomes treated in this manner were tested for effects on fitness in both hemizygous and heterozygous conditions, and for effects on viability in hemizygous and homozygous conditions. In addition, untreated X chromosomes were available for study. The viability and heterozygous fitness effects are presented in this paper, and the hemizygous fitness effects are discussed in the accompanying one (Mitchell and Simmons 1977). Hemizygous and homozygous viability effects were measured by segregation tests in vial cultures. For hemizygous males, viability was reduced 0.5 percent per mm EMS treatment; for homozygous females, it was reduced 0.7 percent per mm treatment. The decline in viability appeared to be a linear function of EMS dose. The viabilities of males and females were strongly correlated. Heterozygous fitness effects were measured by monitoring changes in the frequencies of treated and untreated X chromosomes in discrete generation populations which, through the use of an X-Y translocation, maintained them only in heterozygous condition. Flies that were heterozygous for a treated chromosome were found to be 0.4 percent less fit per m m EMS than flies heterozygous for an untreated one.

scholarly journals Behavioral variation in Drosophila melanogaster: no evidence for common alleles of large- effect at the foraging gene in a population from North Carolina, USA

2014 ◽  
Author(s):  
Thomas Turner ◽  
Christopher C Giauque ◽  
Daniel R Schrider ◽  
Andrew D Kern
Keyword(s):  
North Carolina ◽  
Drosophila Melanogaster ◽  
Genetic Variation ◽  
Foraging Behavior ◽  
Additional Data ◽  
Balancing Selection ◽  
Natural Populations ◽  
Specific Population ◽  
Foraging Gene ◽  
Population Genetic Variation

It has been postulated that natural populations of Drosophila melanogaster are comprised of two behavioral morphs termed "rover" and "sitter", and that this variation is caused mainly by large-effect alleles at a single locus. Contrary to common assertions, however, published support for the existence of common large effect alleles in nature is quite limited. To further investigate, we quantified the foraging behavior of 36 sequenced strains from a natural population, performed an association study, and described patterns of molecular evolution at the foraging locus. Though there was significant variation in foraging behavior among genotypes, this variation was continuously distributed and not significantly associated with genetic variation at the foraging gene. Patterns of molecular population genetic variation at this gene also provide no support for the hypothesis that for is a target of recent balancing selection. Though our data only apply to this specific population, we propose that additional data is required to support a hypothesis of common alleles of large effect on foraging behavior in nature.

scholarly journals Dispersal alters the nature and scope of sexually antagonistic variation

2020 ◽  
Author(s):  
Ewan O Flintham ◽  
Vincent Savolainen ◽  
Charles Mullon
Keyword(s):  
Genetic Variation ◽  
Balancing Selection ◽  
Sexual Antagonism ◽  
Previous Theory ◽  
Fitness Effects ◽  
Kin Competition ◽  
Spatial Subdivision ◽  
Subdivided Populations ◽  
Limited Dispersal ◽  
Intralocus Conflict

AbstractIntra-locus sexual conflict, or sexual antagonism, occurs when alleles have opposing fitness effects in the two sexes. Previous theory suggests that sexual antagonism is a driver of genetic variation by generating balancing selection. However, these studies assume that populations are well-mixed, neglecting the effects of spatial subdivision. Here we use mathematical modelling to show that limited dispersal can fundamentally change evolution at sexually antagonistic autosomal and X-linked loci due to inbreeding and sex-specific kin competition. We find that if the sexes disperse at different rates, kin competition within the philopatric sex biases intralocus conflict in favour of the more dispersive sex. Furthermore, kin competition diminishes the strength of balancing selection relative to genetic drift, reducing genetic variation in small subdivided populations. Meanwhile, by decreasing heterozygosity, inbreeding reduces the scope for sexually antagonistic polymorphism due to non-additive allelic effects, and this occurs to a greater extent on the X-chromosome than autosomes. Overall, our results demonstrate that spatial structure is an important factor in predicting where to expect sexually antagonistic alleles. We suggest that observed interspecific and intragenomic variation in sexual antagonism may be explained by sex-specific dispersal ecology and demography.

Heterogeneous Selection at Specific Loci in Natural Environments in Arabidopsis thaliana

Genetics ◽  
2003 ◽  
Vol 165 (1) ◽  
pp. 321-329 ◽  
Author(s):  
Cynthia Weinig ◽  
Lisa A Dorn ◽  
Nolan C Kane ◽  
Zachary M German ◽  
Solveig S Halldorsdottir ◽  
...  
Keyword(s):  
Arabidopsis Thaliana ◽  
Genetic Variation ◽  
Natural Selection ◽  
Rhode Island ◽  
Plant Species ◽  
Allelic Variation ◽  
Balancing Selection ◽  
Wild Plant ◽  
Natural Environments ◽  
Fitness Effects

Abstract Genetic variation for quantitative traits is often greater than that expected to be maintained by mutation in the face of purifying natural selection. One possible explanation for this observed variation is the action of heterogeneous natural selection in the wild. Here we report that selection on quantitative trait loci (QTL) for fitness traits in the model plant species Arabidopsis thaliana differs among natural ecological settings and genetic backgrounds. At one QTL, the allele that enhanced the viability of fall-germinating seedlings in North Carolina reduced the fecundity of spring-germinating seedlings in Rhode Island. Several other QTL experienced strong directional selection, but only in one site and seasonal cohort. Thus, different loci were exposed to selection in different natural environments. Selection on allelic variation also depended upon the genetic background. The allelic fitness effects of two QTL reversed direction depending on the genotype at the other locus. Moreover, alternative alleles at each of these loci caused reversals in the allelic fitness effects of a QTL closely linked to TFL1, a candidate developmental gene displaying nucleotide sequence polymorphism consistent with balancing selection. Thus, both environmental heterogeneity and epistatic selection may maintain genetic variation for fitness in wild plant species.

scholarly journals The evolutionary potential of diet-dependent effects on lifespan and fecundity in a multi-parental population of Drosophila melanogaster

2018 ◽  
Author(s):  
Enoch Ng’oma ◽  
Wilton Fidelis ◽  
Kevin M. Middleton ◽  
Elizabeth G. King
Keyword(s):  
Drosophila Melanogaster ◽  
Genetic Variation ◽  
Genetic Correlations ◽  
Natural Populations ◽  
Evolutionary Potential ◽  
Fitness Components ◽  
Nutrient Imbalance ◽  
Quantitative Genetic ◽  
Nutritional Conditions ◽  
Quantitative Genetic Parameters

AbstractThe nutritional conditions experienced by a population play a major role in shaping trait evolution in many taxa. Constraints exerted by nutrient limitation or nutrient imbalance can influence the maximal value that fitness components such as reproduction and lifespan attains, and organisms may shift how resources are allocated to different structures and functions in response to changes in nutrition. Whether the phenotypic changes associated with changes in nutrition represent an adaptive response is largely unknown. Further, it is unclear whether the response of fitness components to diet even has the potential to evolve in most systems. In this study, we use an admixed multiparental population of Drosophila melanogaster reared in three different diet conditions to estimate quantitative genetic parameters for lifespan and fecundity. We find significant genetic variation for both traits in our population and show that lifespan has moderate to high heritabilities within diets. Genetic correlations for lifespan between diets were significantly less than one, demonstrating a strong genotype by diet interaction. These findings demonstrate substantial standing genetic variation in our population that is comparable to natural populations and highlights the potential for adaptation to changing nutritional environments.

scholarly journals Genetic variation for expression of the sex determination pathway genes in Drosophila melanogaster

2005 ◽  
Vol 86 (1) ◽  
pp. 31-40 ◽  
Author(s):  
AARON M. TARONE ◽  
YASEEN M. NASSER ◽  
SERGEY V. NUZHDIN
Keyword(s):  
Drosophila Melanogaster ◽  
Genetic Variation ◽  
Sex Determination ◽  
Transcript Level ◽  
Morphological Characters ◽  
Adult Males ◽  
Transcript Levels ◽  
Downstream Target ◽  
Trade Offs ◽  
Males And Females

Sequence polymorphisms result in phenotypic variation through the pathways of interacting genes and their products. We focused on transcript-level variation in the splicing pathway for sex determination – a model network defining downstream morphological characters that are dimorphic between males and females. Expression of Sex lethal, transformer, transformer2, doublesex, intersex and hermaphrodite was assayed with quantitative RT-PCR in 0- to 1-day-old adult males and females of 36 Drosophila melanogaster inbred lines. Abundant genetic variation in the transcript levels was found for all genes. Sex-specific splices had high concentrations in the appropriate sex. In the other sex, low but detectable concentrations were also observed. Abundances of splices strongly co-varied between sexes among genotypes, with little genetic variation strictly limited to one sex. The level of sexually dimorphic Yolk protein1 expression – an immediate downstream target of the pathway – was modelled as the target phenotype of the upstream sex determination pathway. Substantial genetic variation in this phenotype in males was explained by leaky splicing of female-specific transcripts. If higher transcript levels of the appropriate isoform of sex determination genes are beneficial in a sex, then stronger leakiness of the inappropriate transcript might be deleterious, perhaps contributing to the fitness trade-offs previously observed between the sexes.

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