Seasonally fluctuating selection can maintain polymorphism at many loci via segregation lift

Most natural populations are affected by seasonal changes in temperature, rainfall, or resource availability. Seasonally fluctuating selection could potentially make a large contribution to maintaining genetic polymorphism in populations. However, previous theory suggests that the conditions for multilocus polymorphism are restrictive. Here, we explore a more general class of models with multilocus seasonally fluctuating selection in diploids. In these models, the multilocus genotype is mapped to fitness in two steps. The first mapping is additive across loci and accounts for the relative contributions of heterozygous and homozygous loci—that is, dominance. The second step uses a nonlinear fitness function to account for the strength of selection and epistasis. Using mathematical analysis and individual-based simulations, we show that stable polymorphism at many loci is possible if currently favored alleles are sufficiently dominant. This general mechanism, which we call “segregation lift,” requires seasonal changes in dominance, a phenomenon that may arise naturally in situations with antagonistic pleiotropy and seasonal changes in the relative importance of traits for fitness. Segregation lift works best under diminishing-returns epistasis, is not affected by problems of genetic load, and is robust to differences in parameters across loci and seasons. Under segregation lift, loci can exhibit conspicuous seasonal allele-frequency fluctuations, but often fluctuations may be small and hard to detect. An important direction for future work is to formally test for segregation lift in empirical data and to quantify its contribution to maintaining genetic variation in natural populations.

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Segregation lift: A general mechanism for the maintenance of polygenic variation under seasonally fluctuating selection

10.1101/115444 ◽

2017 ◽

Author(s):

Meike J. Wittmann ◽

Alan O. Bergland ◽

Marcus W. Feldman ◽

Paul S. Schmidt ◽

Dmitri A. Petrov

Keyword(s):

Seasonal Changes ◽

Natural Populations ◽

Genetic Load ◽

General Mechanism ◽

Large Contribution ◽

Fluctuating Selection ◽

Previous Theory ◽

Increasing Function ◽

Special Case ◽

Polygenic Variation

AbstractMost natural populations are affected by seasonal changes in temperature, rainfall, or resource availability. Seasonally fluctuating selection could potentially make a large contribution to maintaining genetic polymorphism in populations. However, previous theory suggests that the conditions for multi-locus polymorphism are restrictive. Here we explore a more general class of models with multi-locus seasonally fluctuating selection in diploids. In these models, loci first contribute additively to a seasonal score, with a dominance parameter determining the relative contributions of heterozygous and homozygous loci. The seasonal score is then mapped to fitness via a monotonically increasing function, thereby accounting for epistasis. Using mathematical analysis and individual-based simulations, we show that stable polymorphism at many loci is possible if currently favored alleles are sufficiently dominant with respect to the additive seasonal score (but not necessarily with respect to fitness itself). This general mechanism, which we call “segregation lift”, operates for various genotype-to-fitness maps and includes the previously known mechanism of multiplicative selection with marginal overdominance as a special case. We show that segregation lift may arise naturally in situations with antagonistic pleiotropy and seasonal changes in the relative importance of traits for fitness. Segregation lift is not affected by problems of genetic load and is robust to differences in parameters across loci and seasons. Under segregation lift, loci can exhibit conspicuous seasonal allele-frequency fluctuations, but often fluctuations may also be small and hard to detect. Via segregation lift, seasonally fluctuating selection might contribute substantially to maintaining genetic variation in natural populations.

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CHROMOSOME INTERACTIONS IN DROSOPHILA MELANOGASTER. II. TOTAL FITNESS

Genetics ◽

10.1093/genetics/102.3.485 ◽

1982 ◽

Vol 102 (3) ◽

pp. 485-502

Author(s):

Robert D Seager ◽

Francisco J Ayala ◽

R William Marks

Keyword(s):

Drosophila Melanogaster ◽

Threshold Model ◽

Fitness Function ◽

Natural Populations ◽

Genetic Load ◽

Chromosome 2 ◽

Synergistic Interactions ◽

The Third ◽

Mean Fitness ◽

Selective Maintenance

ABSTRACT In a large experiment, using nearly 200 population cages, we have measured the fitness of Drosophila melanogaster homozygous (1) for the second chromosome, (2) for the third chromosome, and (3) for both chromosomes. Twentyfour second chromosomes and 24 third chromosomes sampled from a natural population were tested. The mean fitness of the homozygous flies is 0.081 ± 0.014 for the second chromosome, 0.080 ± 0.017 for the third chromosome, and 0.079 ± 0.024 for both chromosomes simultaneously. Assuming that fitnesses are multiplicative (the additive fitness model makes no sense in the present case because of the large selection coefficients involved), the expected mean fitness of the homozygotes for both chromosomes is 0.0066; their observed fitness is more than ten times greater. Thus, it appears that synergistic interactions between loci are considerable; and that, consequently, the fitness function substantially departs from linearity. Two models are tentatively suggested for the fitness function: a "threshold" model and a "synergistic" model.—The experiments reported here confirm previous results showing that the concealed genetic load present in natural populations of Drosophila is sufficient to account for the selective maintenance of numerous polymorphisms (of the order of 1000).

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GENETIC LOAD IN NATURAL POPULATIONS: IS IT COMPATIBLE WITH THE HYPOTHESIS THAT MANY POLYMORPHISMS ARE MAINTAINED BY NATURAL SELECTION?

Genetics ◽

10.1093/genetics/77.3.569 ◽

1974 ◽

Vol 77 (3) ◽

pp. 569-589

Author(s):

Martin L Tracey ◽

Francisco J Ayala

Keyword(s):

Drosophila Melanogaster ◽

Natural Selection ◽

Natural Population ◽

Natural Populations ◽

Genetic Load ◽

Structural Genes ◽

Invertebrate Species ◽

Average Proportion ◽

Mean Fitness ◽

The Mean

ABSTRACT Recent studies of genetically controlled enzyme variation lead to an estimation that at least 30 to 60% of the structural genes are polymorphic in natural populations of many vertebrate and invertebrate species. Some authors have argued that a substantial proportion of these polymorphisms cannot be maintained by natural selection because this would result in an unbearable genetic load. If many polymorphisms are maintained by heterotic natural selection, individuals with much greater than average proportion of homozygous loci should have very low fitness. We have measured in Drosophila melanogaster the fitness of flies homozygous for a complete chromosome relative to normal wild flies. A total of 37 chromosomes from a natural population have been tested using 92 experimental populations. The mean fitness of homozygous flies is 0.12 for second chromosomes, and 0.13 for third chromosomes. These estimates are compatible with the hypothesis that many (more than one thousand) loci are maintained by heterotic selection in natural populations of D. melanogaster.

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Detected Changes in Precipitation Extremes at Their Native Scales Derived from In Situ Measurements

Journal of Climate ◽

10.1175/jcli-d-19-0077.1 ◽

2019 ◽

Vol 32 (23) ◽

pp. 8087-8109 ◽

Cited By ~ 2

Author(s):

Mark D. Risser ◽

Christopher J. Paciorek ◽

Travis A. O’Brien ◽

Michael F. Wehner ◽

William D. Collins

Keyword(s):

Extreme Precipitation ◽

Seasonal Changes ◽

Signal To Noise Ratio ◽

Statistical Technique ◽

In Situ Measurements ◽

Absolute Sense ◽

Underlying Causes ◽

Changes Over Time ◽

Future Work

Abstract The gridding of daily accumulated precipitation—especially extremes—from ground-based station observations is problematic due to the fractal nature of precipitation, and therefore estimates of long period return values and their changes based on such gridded daily datasets are generally underestimated. In this paper, we characterize high-resolution changes in observed extreme precipitation from 1950 to 2017 for the contiguous United States (CONUS) based on in situ measurements only. Our analysis utilizes spatial statistical methods that allow us to derive gridded estimates that do not smooth extreme daily measurements and are consistent with statistics from the original station data while increasing the resulting signal-to-noise ratio. Furthermore, we use a robust statistical technique to identify significant pointwise changes in the climatology of extreme precipitation while carefully controlling the rate of false positives. We present and discuss seasonal changes in the statistics of extreme precipitation: the largest and most spatially coherent pointwise changes are in fall (SON), with approximately 33% of CONUS exhibiting significant changes (in an absolute sense). Other seasons display very few meaningful pointwise changes (in either a relative or absolute sense), illustrating the difficulty in detecting pointwise changes in extreme precipitation based on in situ measurements. While our main result involves seasonal changes, we also present and discuss annual changes in the statistics of extreme precipitation. In this paper we only seek to detect changes over time and leave attribution of the underlying causes of these changes for future work.

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Fluctuating selection: the perpetual renewal of adaptation in variable environments

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0150 ◽

2010 ◽

Vol 365 (1537) ◽

pp. 87-97 ◽

Cited By ~ 250

Author(s):

Graham Bell

Keyword(s):

Natural Selection ◽

Evolutionary Biology ◽

Natural Populations ◽

Phenotypic Variance ◽

Weak Selection ◽

Fluctuating Selection ◽

Environmental Variance ◽

Strong Selection ◽

Genomic Studies ◽

Over Time

Darwin insisted that evolutionary change occurs very slowly over long periods of time, and this gradualist view was accepted by his supporters and incorporated into the infinitesimal model of quantitative genetics developed by R. A. Fisher and others. It dominated the first century of evolutionary biology, but has been challenged in more recent years both by field surveys demonstrating strong selection in natural populations and by quantitative trait loci and genomic studies, indicating that adaptation is often attributable to mutations in a few genes. The prevalence of strong selection seems inconsistent, however, with the high heritability often observed in natural populations, and with the claim that the amount of morphological change in contemporary and fossil lineages is independent of elapsed time. I argue that these discrepancies are resolved by realistic accounts of environmental and evolutionary changes. First, the physical and biotic environment varies on all time-scales, leading to an indefinite increase in environmental variance over time. Secondly, the intensity and direction of natural selection are also likely to fluctuate over time, leading to an indefinite increase in phenotypic variance in any given evolving lineage. Finally, detailed long-term studies of selection in natural populations demonstrate that selection often changes in direction. I conclude that the traditional gradualist scheme of weak selection acting on polygenic variation should be supplemented by the view that adaptation is often based on oligogenic variation exposed to commonplace, strong, fluctuating natural selection.

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“Genetic Load”: How the Architects of the Modern Synthesis Became Trapped in a Scientific Ideology

Transversal International Journal for the Historiography of Science ◽

10.24117/2526-2270.2018.i4.11 ◽

2018 ◽

pp. 118

Author(s):

Alexandra Soulier

Keyword(s):

Theoretical Basis ◽

Policy Making ◽

Natural Populations ◽

Genetic Load ◽

Social Progress ◽

Human Populations ◽

Complex Phenomenon ◽

Science And Policy ◽

Theodosius Dobzhansky ◽

Combined Actions

The term “genetic load” first emerged in a paper written in 1950 by the geneticist H. Muller. It is a mathematical model based on biological, social, political and ethical arguments describing the dramatic accumulation of disadvantageous mutations in human populations that will occur in modern societies if eugenic measures are not taken. The model describes how the combined actions of medical and social progress will supposedly impede natural selection and make genes of inferior quality likely to spread across populations – a process which in fine loads their progress. Genetic load is based on optimal fitness and emerges from a “typological view” of evolution. This model of evolution had previously, however, been invalidated by Robert Wright and Theodosius Dobzhansky who, as early as 1946, showed that polymorphism was the rule in natural populations. The blooming and persistence of the concept of genetic load, after its theoretical basis had already expired, are a historical puzzle. This persistence reveals the intricacy of science and policy-making in eugenic matters. The Canguilhemian concept of ‘scientific ideology’ (1988) is used along with the concept of ‘immutable mobile’ (Latour 1986) and compared with the concept of ‘co-production’ (Jasanoff 1998), to provide complementary perspectives on this complex phenomenon.

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POLYMORPHISM IN A CYCLIC PARTHENOGENETIC SPECIES: SIMOCEPHALUS SERRULATUS

Genetics ◽

10.1093/genetics/84.3.631 ◽

1976 ◽

Vol 84 (3) ◽

pp. 631-637

Author(s):

M Yao Smith ◽

Alex Fraser

Keyword(s):

Seasonal Changes ◽

Natural Populations ◽

Genetic Homogeneity ◽

Laboratory Population ◽

Gametic Disequilibrium ◽

Polymorphic Loci ◽

Parthenogenetic Species ◽

Apomictic Parthenogenesis ◽

Isozyme Loci ◽

Electrophoretic Techniques

ABSTRACT A survey of sixteen isozyme loci using electrophoretic techniques was conducted for three isolated natural populations and one laboratory population of the cyclic parthenogenetic species, Simocephalus serrulatus. The proportion of polymorphic loci (33%-60%) and the average number of heterozygous loci per individual (6%-23%) in the three natural populations were found to be comparable to those found in most sexually reproducing organisms. Detailed analyses were made for one of these populations using five polymorphic loci. The results indicated that (1) seasonal changes in genotypic frequencies took place, (2) apomictic parthenogenesis does not lead to genetic homogeneity, and (3) marked gametic disequilibrium at these five loci was present in the population, indicating that selection acted on coadapted groups of genes.

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