An official website of the United States government
Infectious disease can threaten host populations. Hosts can rapidly evolve resistance during epidemics, with this evolution often modulated by fitness trade-offs (e.g., between resistance and fecundity). However, many organisms switch between asexual and sexual reproduction, and this shift in reproductive strategy can also alter how resistance in host populations persists through time. Recombination can shuffle alleles selected for during an asexual phase, uncoupling the combinations of alleles that facilitated resistance to parasites and altering the distribution of resistance phenotypes in populations. Furthermore, in host species that produce diapausing propagules (e.g., seeds, spores, or resting eggs) after sex, accumulation of propagules into and gene flow out of a germ bank introduce allele combinations from past populations. Thus, recombination and gene flow might shift populations away from the trait distribution reached after selection by parasites. To understand how recombination and gene flow alter host population resistance, we tracked the genotypic diversity and resistance distributions of two wild populations of cyclical parthenogens. In one population, resistance and genetic diversity increased after recombination whereas, in the other, recombination did not shift already high resistance and genetic diversity. In both lakes, resistance remained high after temporal gene flow. This observation surprised us: due to costs to resistance imposed by a fecundity-resistance trade-off, we expected that high population resistance would be a transient state that would be eroded through time by recombination and gene flow. Instead, low resistance was the transient state, while recombination and gene flow re-established or maintained high resistance to this virulent parasite. We propose this outcome may have been driven by the joint influence of fitness trade-offs, genetic slippage after recombination, and temporal gene flow via the egg bank.
more »
« less
Gene flow accelerates adaptation to a parasite
Abstract Gene flow into populations can increase additive genetic variation and introduce novel beneficial alleles, thus facilitating adaptation. However, gene flow may also impede adaptation by disrupting beneficial genotypes, introducing deleterious alleles, or creating novel dominant negative interactions. While theory and fieldwork have provided insight as to the effects of gene flow, direct experimental tests are rare. Here, we evaluated the effects of gene flow on adaptation in the nematode Caenorhabditis elegans during exposure to the bacterial parasite Serratia marcescens. We evolved hosts against non-evolving parasites for ten passages while controlling host gene flow and source population. We used source nematode populations with three different genetic backgrounds (one similar to the sink population and two different) and two evolutionary histories (previously adapted to S. marcescens or naïve). We found that populations with gene flow exhibited greater increases in parasite resistance than those without gene flow. Additionally, gene flow from adapted populations resulted in greater increases in resistance than gene flow from naïve populations, particularly with gene flow from novel genetic backgrounds. Overall, this work demonstrates that gene flow can facilitate adaptation, and suggests that the genetic architecture and evolutionary history of source populations can alter the sink population’s response to selection.
more »
« less
- PAR ID:
- 10405867
- Date Published:
- Journal Name:
- Evolution
- ISSN:
- 0014-3820
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Host populations often evolve defenses against parasites due to the significant fitness costs imposed by infection. However, adaptation to a specific parasite may alter the effectiveness of the host’s defenses in general. Consequently, the specificity of host defense may be influenced by a host population’s evolutionary history with parasites. Further, the degree of reciprocal change within an interaction may profoundly alter the range of host defense, given that antagonistic coevolutionary interactions are predicted to favor defense against specific parasite genotypes. Here, we examined the effect of host evolutionary history on host defense range by assessing the mortality rates of Caenorhabditis elegans host populations exposed to an array of Serratia marcescens bacterial parasite strains. Importantly, each of the host populations were derived from the same genetic background but have different experimental evolution histories with parasites. Each of these histories (exposure to either heat-killed, fixed genotype, or coevolving parasites) carries a different level of evolutionary reciprocity. Overall, we observed an effect of host evolutionary history in that previously coevolved host populations were generally the most susceptible to novel parasite strains. This data demonstrates that host evolutionary history can have a significant impact on host defense, and that host-parasite coevolution can increase host susceptibility to novel parasites.more » « less
-
Following severe environmental change that reduces mean population fitness below replacement, populations must adapt to avoid eventual extinction, a process called evolutionary rescue. Models of evolutionary rescue demonstrate that initial size, genetic variation and degree of maladaptation influence population fates. However, many models feature populations that grow without negative density dependence or with constant genetic diversity despite precipitous population decline, assumptions likely to be violated in conservation settings. We examined the simultaneous influences of density-dependent growth and erosion of genetic diversity on populations adapting to novel environmental change using stochastic, individual-based simulations. Density dependence decreased the probability of rescue and increased the probability of extinction, especially in large and initially well-adapted populations that previously have been predicted to be at low risk. Increased extinction occurred shortly following environmental change, as populations under density dependence experienced more rapid decline and reached smaller sizes. Populations that experienced evolutionary rescue lost genetic diversity through drift and adaptation, particularly under density dependence. Populations that declined to extinction entered an extinction vortex, where small size increased drift, loss of genetic diversity and the fixation of maladaptive alleles, hindered adaptation and kept populations at small densities where they were vulnerable to extinction via demographic stochasticity.more » « less
-
Abstract Loss-of-function alleles are a pertinent source of genetic variation with the potential to contribute to adaptation. Cave-adapted organisms exhibit striking loss of ancestral traits such as eyes and pigment, suggesting that loss-of-function alleles may play an outsized role in these systems. Here, we leverage 141 whole genome sequences to evaluate the evolutionary history and adaptive potential of single nucleotide premature termination codons (PTCs) in Mexican tetra. We find that cave populations contain significantly more PTCs at high frequency than surface populations. We also find that PTCs occur more frequently in genes with inherent relaxed evolutionary constraint relative to the rest of the genome. Using SLiM to simulate PTC evolution in a cavefish population, we show that the smaller population size and increased genetic drift is sufficient to account for the observed increase in PTC frequency in cave populations without positive selection. Using CRISPR-Cas9, we show that mutation of one of these genes, pde6c, produces phenotypes in surface Mexican tetra that mimic cave-derived traits. Finally, we identify a small subset of candidate genes that contain high-frequency PTCs in cave populations, occur within selective sweeps, and may contribute to beneficial traits such as reduced energy expenditure, suggesting that a handful of PTCs may be adaptive. Overall, our work provides a rare characterization of PTCs across wild populations and finds that they may have an important role in loss-of-function phenotypes, contributing to a growing body of literature showing genome evolution through relaxed constraint in subterranean organisms.more » « less
-
Shimada, Tomohiro (Ed.)Understanding the interplay between genotype and fitness is a core question in evolutionary biology. Here, we address this challenge in the context of microbial adaptation to environmental stressors. This study explores the role of epistasis in bacterial adaptation by examining genetic and phenotypic changes in silver-adapted Escherichia coli populations, focusing on the role of beneficial mutations in two-component response systems (TCRS). To do this, we measured 24-hour growth assays and conducted whole-genome DNA and RNA sequencing on E. coli mutants that confer resistance to ionic silver. We showed recently that the R15L cusS mutation is central to silver resistance, primarily through upregulation of the cus efflux system. However, here we show that this mutation’s effectiveness is significantly enhanced by epistatic interactions with additional mutations in regulatory genes such as ompR, rho, and fur. These interactions reconfigure global stress response networks, resulting in robust and varied resistance strategies across different populations. This study underscores the critical role of epistasis in bacterial adaptation, illustrating how interactions between multiple mutations and how genetic backgrounds shape the resistance phenotypes of E. coli populations. This work also allowed for refinement of our model describing the role TCRS genes play in bacterial adaptation by now emphasizing that adaptation to environmental stressors is a complex, context-dependent process, driven by the dynamic interplay between genetic and environmental factors. These findings have broader implications for understanding microbial evolution and developing strategies to combat antimicrobial resistance.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/evolut/qpad048
