An official website of the United States government
Abstract Host–parasite interactions may often be subject to opposing evolutionary forces, which likely influence the evolutionary trajectories of both partners. Natural selection and genetic drift are two major evolutionary forces that act in host and parasite populations. Further, population size is a significant determinant of the relative strengths of these forces. In small populations, drift may undermine the persistence of beneficial alleles, potentially impeding host adaptation to parasites. Here, we investigate two questions: (a) can selection pressure for increased resistance in small, susceptible host populations overcome the effects of drift and (b) can resistance be maintained in small host populations? To answer these questions, we experimentally evolved the hostCaenorhabditis elegansagainst its bacterial parasite,Serratia marcescens, for 13 host generations. We found that strong selection favouring increased host resistance was insufficient to counteract drift in small populations, resulting in persistently high host mortality. Additionally, in small populations of resistant hosts, we found that selection for the maintenance of resistance is not always sufficient to curb the loss of resistance. We compared these results with selection in large host populations. We found that initially resistant, large host populations were able to maintain high levels of resistance. Likewise, initially susceptible, large host populations were able to gain resistance to the parasite. These results show that strong selection pressure for survival is not always sufficient to counteract drift. In consideration ofC.elegans natural population dynamics, we suggest that drift may often impede selection in nature.
more »
« less
Interrogating the Roles of Mutation–Selection Balance, Heterozygote Advantage, and Linked Selection in Maintaining Recessive Lethal Variation in Natural Populations
For nearly a century, evolutionary biologists have observed chromosomes that cause lethality when made homozygous persisting at surprisingly high frequencies (>25%) in natural populations of many species. The evolutionary forces responsible for the maintenance of such detrimental mutations have been heavily debated—are some lethal mutations under balancing selection? We suggest that mutation–selection balance alone cannot explain lethal variation in nature and the possibility that other forces play a role. We review the potential that linked selection in particular may drive maintenance of lethal alleles through associative overdominance or linkage to beneficial mutations or by reducing effective population size. Over the past five decades, investigation into this mystery has tapered. During this time, key scientific advances have provided the ability to collect more accurate data and analyze them in new ways, making the underlying genetic bases and evolutionary forces of lethal alleles timely for study once more. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 11 is February 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
more »
« less
- Award ID(s):
- 2019789
- PAR ID:
- 10381994
- Date Published:
- Journal Name:
- Annual Review of Animal Biosciences
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2165-8102
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Natural selection drives adaptive evolution and removes deleterious mutations; these effects are countervailing when a complex adaptation requires mutations that are initially deleterious when they arise, but beneficial in combination. While many models of this dynamic consider how genetic drift or other influences can aid valley crossing by weakening selection, we lack a general, analytical treatment of when relaxed selection might speed this type of adaptation. Here we use simulation and analysis to show that relaxed selection is generally favorable for valley-crossing when adaptive pathways require more than a single deleterious step. We also demonstrate that spatial heterogeneity in selection pressures could, by relaxing selection, allow populations to cross valleys much more rapidly than expected. These results relate to several applications of evolutionary theory to complex systems ranging from host-pathogen evolution to search algorithms in computer science.more » « less
-
Wittkopp, Patricia (Ed.)Abstract Whole-genome duplications (WGDs) have occurred in many eukaryotic lineages. However, the underlying evolutionary forces and molecular mechanisms responsible for the long-term retention of gene duplicates created by WGDs are not well understood. We employ a population-genomic approach to understand the selective forces acting on paralogs and investigate ongoing duplicate-gene loss in multiple species of Paramecium that share an ancient WGD. We show that mutations that abolish protein function are more likely to be segregating in retained WGD paralogs than in single-copy genes, most likely because of ongoing nonfunctionalization post-WGD. This relaxation of purifying selection occurs in only one WGD paralog, accompanied by the gradual fixation of nonsynonymous mutations and reduction in levels of expression, and occurs over a long period of evolutionary time, “marking” one locus for future loss. Concordantly, the fitness effects of new nonsynonymous mutations and frameshift-causing indels are significantly more deleterious in the highly expressed copy compared with their paralogs with lower expression. Our results provide a novel mechanistic model of gene duplicate loss following WGDs, wherein selection acts on the sum of functional activity of both duplicate genes, allowing the two to wander in expression and functional space, until one duplicate locus eventually degenerates enough in functional efficiency or expression that its contribution to total activity is too insignificant to be retained by purifying selection. Retention of duplicates by such mechanisms predicts long times to duplicate-gene loss, which should not be falsely attributed to retention due to gain/change in function.more » « less
-
Barluenga, Marta (Ed.)Abstract Trait loss represents an intriguing evolutionary problem, particularly when it occurs across independent lineages. Fishes in light-poor environments often evolve “troglomorphic” traits, including reduction or loss of both pigment and eyes. Here, we investigate the genomic basis of trait loss in a blind and depigmented African cichlid, Lamprologus lethops, and explore evolutionary forces (selection and drift) that may have contributed to these losses. This species, the only known blind cichlid, is endemic to the lower Congo River. Available evidence suggests that it inhabits deep, low-light habitats. Using genome sequencing, we show that genes related to eye formation and pigmentation, as well as other traits associated with troglomorphism, accumulated inactivating mutations rapidly after speciation. A number of the genes affected in L. lethops are also implicated in troglomorphic phenotypes in Mexican cavefish (Astyanax mexicanus) and other species. Analysis of heterozygosity patterns across the genome indicates that L. lethops underwent a significant population bottleneck roughly 1 Ma, after which effective population sizes remained low. Branch-length tests on a subset of genes with inactivating mutations show little evidence of directional selection; however, low overall heterozygosity may reduce statistical power to detect such signals. Overall, genome-wide patterns suggest that accelerated genetic drift from a severe bottleneck, perhaps aided by directional selection for the loss of physiologically expensive traits, caused inactivating mutations to fix rapidly in this species.more » « less
-
Trait loss represents an intriguing evolutionary problem, particularly when it occurs across independent lineages. Fishes in light-poor environments often evolve “troglomorphic” traits, including reduction or loss of both pigment and eyes. Here, we investigate the genomic basis of trait loss in a blind and depigmented African cichlid, Lamprologus lethops, and explore evolutionary forces (selection and drift) that may have contributed to these losses. This species, the only known blind cichlid, is endemic to the lower Congo River. Available evidence suggests that it inhabits deep, low-light habitats. Using genome sequencing, we show that genes related to eye formation and pigmentation, as well as other traits associated with troglomorphism, accumulated inactivating mutations rapidly after speciation. A number of the genes affected in L. lethops are also implicated in troglomorphic phenotypes in Mexican cavefish(Astyanax mexicanus) and other species. Analysis of heterozygosity patterns across the genome indicates that L. lethops underwent significant population bottleneck roughly 1Ma, after which effective population sizes remained low. Branch-length tests on a subset of genes with inactivating mutations show little evidence of directional selection; however, low overall heterozygosity may reduce statistical power to detect such signals. Overall, genome-wide patterns suggest that accelerated genetic drift from a severe bottleneck, perhaps aided by directional selection for the loss of physiologically expensive traits, caused inactivating mutations to fix rapidly in this species.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1146/annurev-animal-050422-092520
