scholarly journals Compensatory evolution via cryptic genetic variation: Distinct trajectories to phenotypic and fitness recovery

2017 ◽  
Author(s):  
Sudarshan Chari ◽  
Christian Marier ◽  
Cody Porter ◽  
Emmalee Northrop ◽  
Alexandra Belinky ◽  
...  

AbstractPopulations are constantly exposed to deleterious alleles, most of which are purged via natural selection. However, deleterious fitness effects of alleles can also be suppressed by compensatory adaptation. Compensatory mutations can act directly to reduce deleterious effects of an allele. Alternatively, compensation may also occur by altering other aspects of an organisms’ phenotype or performance, without suppressing the phenotypic effects of the deleterious allele. Moreover, the origin of allelic variation contributing to compensatory adaptation remains poorly understood. Compensatory evolution driven by mutations that arise during the selective process are well studied. However less is known about the role standing (cryptic) genetic variation plays in compensatory adaptation. To address these questions, we examined evolutionary trajectories of natural populations of Drosophila melanogaster fixed for mutations that disrupt wing morphology, resulting in deleterious effects on several components of fitness. Lineages subjected only to natural selection, evolved modifications to courtship behavior and several life history traits without compensation in wing morphology. Yet, we observed rapid phenotypic compensation of wing morphology under artificial selection, consistent with segregating variation for compensatory alleles. We show that alleles contributing to compensation of wing morphology have deleterious effects on other fitness components. These results demonstrate the potential for multiple independent avenues for rapid compensatory adaptation from standing genetic variation, which ultimately may reveal novel adaptive trajectories.

2019 ◽  
Author(s):  
Christopher H. Chandler ◽  
Anna Mammel ◽  
Ian Dworkin

AbstractTheoretical work predicts that sexual selection can enhance natural selection, increasing the rate of adaptation to new environments and helping purge harmful mutations. While some experiments support these predictions, remarkably little work has addressed the role of sexual selection on compensatory adaptation—populations’ ability to compensate for the costs of deleterious alleles that are already present. We tested whether sexual selection, as well as the degree of standing genetic variation, affect the rate of compensatory evolution via phenotypic suppression in experimental populations ofDrosophila melanogaster. These populations were fixed for a spontaneous mutation causing mild abnormalities in the male sex comb, a structure important for mating success. We fine-mapped this mutation to an ∼85 kb region on the X chromosome containing three candidate genes, showed that the mutation is deleterious, and that its phenotypic expression and penetrance vary by genetic background. We then performed experimental evolution, including a treatment where opportunity for mate choice was limited by experimentally enforced monogamy. Although evolved populations did show some phenotypic suppression of the morphological abnormalities in the sex comb, the amount of suppression did not depend on the opportunity for sexual selection. Sexual selection, therefore, may not always enhance natural selection; instead, the interaction between these two forces may depend on additional factors.


Genetics ◽  
1992 ◽  
Vol 130 (2) ◽  
pp. 355-366
Author(s):  
H Hollocher ◽  
A R Templeton ◽  
R DeSalle ◽  
J S Johnston

Abstract Natural populations of Drosophila mercatorum are polymorphic for a phenotypic syndrome known as abnormal abdomen (aa). This syndrome is characterized by a slow-down in egg-to-adult developmental time, retention of juvenile abdominal cuticle in the adult, increased early female fecundity, and decreased adult longevity. Previous studies revealed that the expression of this syndrome in females is controlled by two closely linked X chromosomal elements: the occurrence of an R1 insert in a third or more of the X-linked 28S ribosomal genes (rDNA), and the failure of replicative selection favoring uninserted 28S genes in larval polytene tissues. The expression of this syndrome in males in a laboratory stock was associated with the deletion of the rDNA normally found on the Y chromosome. In this paper we quantify the levels of genetic variation for these three components in a natural population of Drosophila mercatorum found near Kamuela, Hawaii. Extensive variation is found in the natural population for both of the X-linked components. Moreover, there is a significant association between variation in the proportion of R1 inserted 28S genes with allelic variation at the underreplication (ur) locus such that both of the necessary components for aa expression in females tend to cosegregate in the natural population. Accordingly, these two closely linked X chromosomal elements are behaving as a supergene in the natural population. Because of this association, we do not believe the R1 insert to be actively transposing to an appreciable extent. The Y chromosomes extracted from nature are also polymorphic, with 16% of the Ys lacking the Y-specific rDNA marker. The absence of this marker is significantly associated with the expression of aa in males. Hence, all three of the major genetic determinants of the abnormal abdomen syndrome are polymorphic in this natural population.


2020 ◽  
Vol 10 (5) ◽  
pp. 1541-1551
Author(s):  
Christopher H. Chandler ◽  
Anna Mammel ◽  
Ian Dworkin

Theoretical work predicts that sexual selection can enhance natural selection, increasing the rate of adaptation to new environments and helping purge harmful mutations. While some experiments support these predictions, remarkably little work has addressed the role of sexual selection on compensatory adaptation—populations’ ability to compensate for the costs of deleterious alleles that are already present. We tested whether sexual selection, as well as the degree of standing genetic variation, affect the rate of compensatory evolution via phenotypic suppression in experimental populations of Drosophila melanogaster. These populations were fixed for a spontaneous mutation causing mild abnormalities in the male sex comb, a structure important for mating success. We fine-mapped this mutation to an ∼85 kb region on the X chromosome containing three candidate genes, showed that the mutation is deleterious, and that its phenotypic expression and penetrance vary by genetic background. We then performed experimental evolution, including a treatment where opportunity for mate choice was limited by experimentally enforced monogamy. Although evolved populations did show some phenotypic suppression of the morphological abnormalities in the sex comb, the amount of suppression did not depend on the opportunity for sexual selection. Sexual selection, therefore, may not always enhance natural selection; instead, the interaction between these two forces may depend on additional factors.


1972 ◽  
Vol 20 (1) ◽  
pp. 19-42 ◽  
Author(s):  
Francisco J. Ayala ◽  
Jeffrey R. Powell ◽  
Martin L. Tracey

SUMMARYWe have studied genetic variation at 27 loci in 42 samples from natural populations of a neotropical species, Drosophila equinoxialis, using standard techniques of starch-gel electrophoresis to detect allelic variation in genes coding for enzymes. There is considerarle genetic variability in D. equinoxialis. We have found allelic variation in each of the 27 loci, although not in every population. On the average, 71% of the loci are polymorphic – that is, the most common allele has a frequency no greater than 0·95 – in a given population. An individual is heterozygous on the average at 21·8% of its loci.The amount of genetic variation fluctuates widely from locus to locus. At the Mdh-2 locus arout 1% of the individuals are heterozygotes; at the other extreme more than 56% of the individuals are heterozygous at the Est-3. At any given locus the configuration of allelic frequencies is strikingly similar from locality to locality. At each and every locus the same allele is generally the most common throughout the distribution of the species. Yet differences in gene frequencies occur between localities. The pattern of genetic variation is incompatible with the hypothesis that the variation is adaptively neutral. Genetic variation in D. equinoxialis is maintained by balancing natural selection.The amount and pattern of genetic variation is similar in D. equinoxialis and its sibling species, D. willistoni. Yet the two species are genetically very different. Different sets of alleles occur at nearly 40% of the loci.


2014 ◽  
Vol 54 (5) ◽  
pp. 783-793 ◽  
Author(s):  
C. C. Ledon-Rettig ◽  
D. W. Pfennig ◽  
A. J. Chunco ◽  
I. Dworkin

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Wen Huang ◽  
Richard F Lyman ◽  
Rachel A Lyman ◽  
Mary Anna Carbone ◽  
Susan T Harbison ◽  
...  

Mutation and natural selection shape the genetic variation in natural populations. Here, we directly estimated the spontaneous mutation rate by sequencing new Drosophila mutation accumulation lines maintained with minimal natural selection. We inferred strong stabilizing natural selection on quantitative traits because genetic variation among wild-derived inbred lines was much lower than predicted from a neutral model and the mutational effects were much larger than allelic effects of standing polymorphisms. Stabilizing selection could act directly on the traits, or indirectly from pleiotropic effects on fitness. However, our data are not consistent with simple models of mutation-stabilizing selection balance; therefore, further empirical work is needed to assess the balance of evolutionary forces responsible for quantitative genetic variation.


Genome ◽  
2002 ◽  
Vol 45 (1) ◽  
pp. 13-21 ◽  
Author(s):  
Bryant F McAllister

Geographically structured genetic variation, as represented by clines and hybrid zones, offers unique opportunities to study adaptation and speciation in natural populations. A hybrid zone has been reported between Drosophila americana americana and Drosophila americana texana, two taxa that are distinguished solely by the arrangement of their X and 4th chromosomes. In this study, samples of D. americana were collected along a latitudinal transect across the inferred hybrid zone, and the frequency of the alternative chromosomal arrangements is reported. These data illustrate that the alternative chromosomal arrangements are distributed along a shallow cline over a broad geographic region, and that the frequency of the arrangements is tightly correlated with latitude. Allelic variants at 13 RFLP loci in three genes on chromosome 4 exhibit no evidence of association with the cline. Presence of a cline for the chromosomal arrangements, as well as a general absence of geographic structure for variation at these genes, is interpreted as evidence that natural selection is responsible for the maintenance of this chromosomal cline. Furthermore, these results demonstrate that taxonomic subdivision of D. americana is unwarranted, because it exists as a cohesive species that is segregating a chromosomal fusion.Key words: chromosomal evolution, Robertsonian fusion, hybrid zone, cline, geographic variation, natural selection.


Genome ◽  
1989 ◽  
Vol 31 (1) ◽  
pp. 296-303 ◽  
Author(s):  
Alan R. Templeton ◽  
Hope Hollocher ◽  
Susan Lawler ◽  
J. Spencer Johnston

Natural populations of Drosophila mercatorum are variable for the number of X-linked 28S ribosomal genes bearing a 5-kilobase insert. A separate polymorphic X-linked gene controls whether 28S repeats bearing the insert are preferentially underreplicated during the formation of polytene tissue. Female flies having at least a third of their 28S genes bearing the insert and lacking the ability to preferentially underreplicate inserted repeats display the abnormal abdomen syndrome. The syndrome is characterized by retention of juvenile abdominal cuticle into the adult, a slowdown in larval developmental time, and an increase in early female fecundity. The life history traits are expressed in nature and provide a basis for strong natural selection. The abnormal abdomen syndrome should be favored whenever the adult age structure is skewed towards young individuals, and field studies confirm this prediction. The closely related species, Drosophila hydei, also bears these inserts and appears to be subject to similar selection. However, D. mercatorum responds to this selection primarily through the allelic variation that controls preferential underreplication, whereas D. hydei responds primarily through adjustment of the proportion of inserted 28S genes. This is interpreted to mean that the evolution of a multigene family arises from the interaction of population-level and DNA-level processes.Key words: ribosomal DNA, natural selection, concerted evolution, life history, multigene families, Drosophila mercatorum, Drosophila hydei.


Genetics ◽  
2002 ◽  
Vol 160 (1) ◽  
pp. 333-342
Author(s):  
Nick Lauter ◽  
John Doebley

Abstract How new discrete states of morphological traits evolve is poorly understood. One possibility is that single-gene changes underlie the evolution of new discrete character states and that evolution is dependent on the occurrence of new single-gene mutations. Another possibility is that multiple-gene changes are required to elevate an individual or population above a threshold required to produce the new character state. A prediction of the latter model is that genetic variation for the traits should exist in natural populations in the absence of phenotypic variation. To test this idea, we studied traits that are phenotypically invariant within teosinte and for which teosinte is discretely different from its near relative, maize. By employing a QTL mapping strategy to analyze the progeny of a testcross between an F1 of two teosintes and a maize inbred line, we identified cryptic genetic variation in teosinte for traits that are invariant in teosinte. We argue that such cryptic genetic variation can contribute to the evolution of novelty when reconfigured to exceed the threshold necessary for phenotypic expression or by acting to modify or stabilize the effects of major mutations.


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