The adaptive function of sexual reproduction: resampling the pool of genotypic possibilities.

Author(s):  
Donal Hickey ◽  
Brian Golding

Abstract BackgroundNatural populations harbor significant levels of genetic variability. Because of this standing genetic variation, the number of possible genotypic combinations is many orders of magnitude greater than the population size. This means that any given population contains only a tiny fraction of all possible genotypic combinations.ResultsWe show that recombination allows a finite population to resample the genotype pool, i.e., the universe of all possible genotypic combinations. Recombination, in combination with natural selection, enables an evolving sexual population to replace existing genotypes with new, higher-fitness genotypic combinations that did not previously exist in the population. Gradually the selected sexual population approaches a state where the optimum genotype is produced by recombination and where it rises to fixation. In contrast to this, an asexual population is limited to selection among existing lower fitness genotypes.ConclusionsThe significance of the result is two-fold. First, it provides an explanation for the ubiquity of sexual reproduction in evolving populations. Secondly, it shows that recombination serves to remove concerns about the cost of natural selection acting on the naturally occurring standing genetic variation. This means that classic population genetics theory is applicable to ecological studies of natural selection acting on standing genetic variation.

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Donal A. Hickey ◽  
G. Brian Golding

Abstract Background Natural populations harbor significant levels of genetic variability. Because of this standing genetic variation, the number of possible genotypic combinations is many orders of magnitude greater than the population size. This means that any given population contains only a tiny fraction of all possible genotypic combinations. Results We show that recombination allows a finite population to resample the genotype pool, i.e., the universe of all possible genotypic combinations. Recombination, in combination with natural selection, enables an evolving sexual population to replace existing genotypes with new, higher-fitness genotypic combinations that did not previously exist in the population. This process allows the sexual population to gradually increase its fitness far beyond the range of fitnesses in the initial population. In contrast to this, an asexual population is limited to selection among existing lower fitness genotypes. Conclusions The results provide an explanation for the ubiquity of sexual reproduction in evolving natural populations, especially when natural selection is acting on the standing genetic variation.


2020 ◽  
Author(s):  
Donal A. Hickey ◽  
G. Brian Golding

AbstractRecombination allows a finite population to resample the genotype pool, i.e., the universe of all possible genotypic combinations. This is important in populations that contain abundant genetic variation because, in such populations, the number of potential genotypes is much larger than the number of individuals in the population. Here, we show how recombination, in combination with natural selection, enables an evolving sexual population to replace existing genotypes with new, higher-fitness genotypic combinations. In contrast to this, an asexual population is limited to selection among existing genotypes. Since it has been shown that most eukaryotic species are genetically polymorphic, our model can explain the ubiquity of sex among such species. The model also indicates that classic population genetics theory is applicable to ecological studies of natural selection acting on standing genetic variation.


Genetics ◽  
1998 ◽  
Vol 150 (2) ◽  
pp. 523-532 ◽  
Author(s):  
Paul E Turner ◽  
Lin Chao

Abstract Sex allows beneficial mutations that occur in separate lineages to be fixed in the same genome. For this reason, the Fisher-Muller model predicts that adaptation to the environment is more rapid in a large sexual population than in an equally large asexual population. Sexual reproduction occurs in populations of the RNA virus φ6 when multiple bacteriophages coinfect the same host cell. Here, we tested the model's predictions by determining whether sex favors more rapid adaptation of φ6 to a bacterial host, Pseudomonas phaseolicola. Replicate populations of φ6 were allowed to evolve in either the presence or absence of sex for 250 generations. All experimental populations showed a significant increase in fitness relative to the ancestor, but sex did not increase the rate of adaptation. Rather, we found that the sexual and asexual treatments also differ because intense intrahost competition between viruses occurs during coinfection. Results showed that the derived sexual viruses were selectively favored only when coinfection is common, indicating that within-host competition detracts from the ability of viruses to exploit the host. Thus, sex was not advantageous because the cost created by intrahost competition was too strong. Our findings indicate that high levels of coinfection exceed an optimum where sex may be beneficial to populations of φ6, and suggest that genetic conflicts can evolve in RNA viruses.


Author(s):  
Ailene MacPherson ◽  
Matthew J. Keeling ◽  
Sarah P. Otto

AbstractCoevolutionary negative frequency dependent selection has been hypothesized to maintain genetic variation in host and parasites. Despite the extensive literature pertaining to host-parasite coevolution, the effect of matching-alleles (MAM) coevolution on the maintenance of genetic variation has not been explicitly modelled in a finite population. The dynamics of the MAM in an infinite population, in fact, suggests that genetic variation in these coevolving populations behaves neutrally. We find that while this is largely true in finite populations two additional phenomena arise. The first of these effects is that of coevolutionary natural selection on stochastic perturbations in host and pathogen allele frequencies. While this may increase or decrease genetic variation, depending on the parameter conditions, the net effect is small relative to that of the second phenomena. Following fixation in the pathogen, the MAM becomes one of directional selection, which in turn rapidly erodes genetic variation in the host. Hence, rather than maintain it, we find that, on average, matching-alleles coevolution depletes genetic variation.


Genome ◽  
2019 ◽  
Vol 62 (11) ◽  
pp. 761-768
Author(s):  
Donal A. Hickey ◽  
G. Brian Golding

The cumulative reproductive cost of multi-locus selection has been considered to be a potentially limiting factor on the rate of adaptive evolution. In this paper, we show that Haldane’s arguments for the accumulation of reproductive costs over multiple loci are valid only for a clonally reproducing population of asexual genotypes. We show that a sexually reproducing population avoids this accumulation of costs. Thus, sex removes a perceived reproductive constraint on the rate of adaptive evolution. The significance of our results is twofold. First, the results demonstrate that adaptation based on multiple genes—such as selection acting on the standing genetic variation—does not entail a huge reproductive cost as suggested by Haldane, provided of course that the population is reproducing sexually. Second, this reduction in the cost of natural selection provides a simple biological explanation for the advantage of sex. Specifically, Haldane’s calculations illustrate the evolutionary disadvantage of asexuality; sexual reproduction frees the population from this disadvantage.


2019 ◽  
Author(s):  
Donal A. Hickey ◽  
G. Brian Golding

AbstractThe cumulative reproductive cost of multi-locus selection has been seen as a potentially limiting factor on the rate of adaptive evolution. In this paper, we show that Haldane’s arguments for the accumulation of reproductive costs over multiple loci are valid only for a clonally reproducing population of asexual genotypes. We show that a sexually reproducing population avoids this accumulation of costs. Thus, sex removes a perceived reproductive constraint on the rate of adaptive evolution. The significance of our results is twofold. First, the results demonstrate that adaptation based on multiple genes – such as selection acting on the standing genetic variation - does not entail a huge reproductive cost as suggested by Haldane, provided of course that the population is reproducing sexually. Secondly, this reduction in the cost of natural selection provides a simple biological explanation for the advantage of sex. Specifically, Haldane’s calculations illustrate the evolutionary disadvantage of asexuality; sexual reproduction frees the population from this disadvantage.


2013 ◽  
Vol 368 (1610) ◽  
pp. 20120080 ◽  
Author(s):  
Graham Bell

Populations subject to severe stress may be rescued by natural selection, but its operation is restricted by ecological and genetic constraints. The cost of natural selection expresses the limited capacity of a population to sustain the load of mortality or sterility required for effective selection. Genostasis expresses the lack of variation that prevents many populations from adapting to stress. While the role of relative fitness in adaptation is well understood, evolutionary rescue emphasizes the need to recognize explicitly the importance of absolute fitness. Permanent adaptation requires a range of genetic variation in absolute fitness that is broad enough to provide a few extreme types capable of sustained growth under a stress that would cause extinction if they were not present. This principle implies that population size is an important determinant of rescue. The overall number of individuals exposed to selection will be greater when the population declines gradually under a constant stress, or is progressively challenged by gradually increasing stress. In gradually deteriorating environments, survival at lethal stress may be procured by prior adaptation to sublethal stress through genetic correlation. Neither the standing genetic variation of small populations nor the mutation supply of large populations, however, may be sufficient to provide evolutionary rescue for most populations.


1992 ◽  
Vol 59 (3) ◽  
pp. 215-225 ◽  
Author(s):  
Ian M. Hastings

SummaryA conflict of interest may arise between intra-cellular genomes and their host cell. The example explicitly investigated is that of a ‘selfish’ mitochondrion which increases its own rate of replication at the cost of reduced metabolic activity which is deleterious to the host cell. The results apply to deleterious cytoplasmic agents in general, such as intracellular parasites. Numerical simulation suggests that selfish mitochondria are able to invade an isogamous sexual population and are capable of reducing its fitness to below “5 % of that prior to their invasion. Their spread is enhanced by decreasing the number of mitotic divisions between meioses, and this may constitute a significant constraint on the evolution of lifecycles. The presence of such deleterious cytoplasmic agents favours a nuclear mutation whose expression prevents cytoplasm from the other gamete entering the zygote at fertilization, resulting in uniparental inheritance of cytoplasm. Such a mutation appears physiologically plausible and can increase in frequency despite its deleterious effect in halving the amount of cytoplasm in the zygote. It is suggested that these were the conditions under which anisogamy evolved. These results have implications for the evolution of sexual reproduction. Standard theory suggests there is no immediate cost of sex, a twofold cost being incurred later as anisogamy evolves. The analysis described here predicts a large, rapid reduction in fitness associated with isogamous sexual reproduction, due to the spread of deleterious cytoplasmic agents with fitness only subsequently rising to a maximum twofold cost as uniparental inheritance of cytoplasm and anisogamy evolve.


2021 ◽  
Vol 288 (1944) ◽  
pp. 20203094
Author(s):  
David Berger ◽  
Josefine Stångberg ◽  
Julian Baur ◽  
Richard J. Walters

Adaptation in new environments depends on the amount of genetic variation available for evolution, and the efficacy by which natural selection discriminates among this variation. However, whether some ecological factors reveal more genetic variation, or impose stronger selection pressures than others, is typically not known. Here, we apply the enzyme kinetic theory to show that rising global temperatures are predicted to intensify natural selection throughout the genome by increasing the effects of DNA sequence variation on protein stability. We test this prediction by (i) estimating temperature-dependent fitness effects of induced mutations in seed beetles adapted to ancestral or elevated temperature, and (ii) calculate 100 paired selection estimates on mutations in benign versus stressful environments from unicellular and multicellular organisms. Environmental stress per se did not increase mean selection on de novo mutation, suggesting that the cost of adaptation does not generally increase in new ecological settings to which the organism is maladapted. However, elevated temperature increased the mean strength of selection on genome-wide polymorphism, signified by increases in both mutation load and mutational variance in fitness. These results have important implications for genetic diversity gradients and the rate and repeatability of evolution under climate change.


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