Abstract Effective population size affects the efficacy of selection, rate of evolution by drift and neutral diversity levels. When species are subdivided into multiple populations connected by gene flow, evolutionary processes can depend on global or local effective population sizes. Theory predicts that high levels of diversity might be maintained by gene flow, even very low levels of gene flow, consistent with species long‐term effective population size, but tests of this idea are mostly lacking. Here, we show thatLycaeidesbutterfly populations maintain low contemporary (variance) effective population sizes (e.g. ~200 individuals) and thus evolve rapidly by genetic drift. However, populations harboured high levels of genetic diversity consistent with an effective population size several orders of magnitude larger. We hypothesized that the differences in the magnitude and variability of contemporary versus long‐term effective population sizes were caused by gene flow of sufficient magnitude to maintain diversity but only subtly affect evolution on generational timescales. Consistent with this hypothesis, we detected low but nontrivial gene flow among populations. Furthermore, using short‐term population‐genomic time‐series data, we documented patterns consistent with predictions from this hypothesis, including a weak but detectable excess of evolutionary change in the direction of the mean (migrant gene pool) allele frequencies across populations and consistency in the direction of allele frequency change over time. The documented decoupling of diversity levels and short‐term change by drift inLycaeideshas implications for our understanding of contemporary evolution and the maintenance of genetic variation in the wild.
more »
« less
Drift, selection and adaptive variation in small populations of a threatened rattlesnake
Abstract An important goal of conservation genetics is to determine if the viability of small populations is reduced by a loss of adaptive variation due to genetic drift. Here, we assessed the impact of drift and selection on direct measures of adaptive variation (toxin loci encoding venom proteins) in the eastern massasauga rattlesnake (Sistrurus catenatus), a threatened reptile that exists in small isolated populations. We estimated levels of individual polymorphism in 46 toxin loci and 1,467 control loci across 12 populations of this species, and compared the results with patterns of selection on the same loci following speciation ofS. catenatusand its closest relative, the western massasauga (S. tergeminus). Multiple lines of evidence suggest that both drift and selection have had observable impacts on standing adaptive variation. In support of drift effects, we found little evidence for selection on toxin variation within populations and a significant positive relationship between current levels of adaptive variation and long‐ and short‐term estimates of effective population size. However, we also observed levels of directional selection on toxin loci among populations that are broadly similar to patterns predicted from interspecific selection analyses that pre‐date the effects of recent drift, and that functional variation in these loci persists despite small short‐term effective sizes. This suggests that much of the adaptive variation present in populations may represent an example of “drift debt,” a nonequilibrium state where present‐day levels of variation overestimate the amount of functional genetic diversity present in future populations.
more »
« less
- PAR ID:
- 10456889
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 29
- Issue:
- 14
- ISSN:
- 0962-1083
- Format(s):
- Medium: X Size: p. 2612-2625
- Size(s):
- p. 2612-2625
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Convergent evolution is often documented in organisms inhabiting isolated environments with distinct ecological conditions and similar selective regimes. Several Central America islands harbor dwarf Boa populations that are characterized by distinct differences in growth, mass, and craniofacial morphology, which are linked to the shared arboreal and feast-famine ecology of these island populations. Using high-density RADseq data, we inferred three dwarf island populations with independent origins and demonstrate that selection, along with genetic drift, has produced both divergent and convergent molecular evolution across island populations. Leveraging whole-genome resequencing data for 20 individuals and a newly annotated Boa genome, we identify four genes with evidence of phenotypically relevant protein-coding variation that differentiate island and mainland populations. The known roles of these genes involved in body growth (PTPRS, DMGDH, and ARSB), circulating fat and cholesterol levels (MYLIP), and craniofacial development (DMGDH and ARSB) in mammals link patterns of molecular evolution with the unique phenotypes of these island forms. Our results provide an important genome-wide example for quantifying expectations of selection and convergence in closely related populations. We also find evidence at several genomic loci that selection may be a prominent force of evolutionary change—even for small island populations for which drift is predicted to dominate. Overall, while phenotypically convergent island populations show relatively few loci under strong selection, infrequent patterns of molecular convergence are still apparent and implicate genes with strong connections to convergent phenotypes.more » « less
-
Shaw, Ruth; Connallon, Tim (Ed.)Abstract Traits that have lost function sometimes persist through evolutionary time. Persistence may occur if there is not enough standing genetic variation for the trait to allow a response to selection, if selection against the trait is weak relative to drift, or if the trait has a residual function. To determine the evolutionary processes shaping whether nonfunctional traits are retained or lost, we investigated short stamens in 16 populations of Arabidopsis thaliana along an elevational cline in northeast Spain. A. thaliana is highly self-pollinating and prior work suggests short stamens do not contribute to self-pollination. We found a cline in short stamen number from retention of short stamens in high-elevation populations to incomplete loss in low-elevation populations. We did not find evidence that limited genetic variation constrains short stamen loss at high elevations, nor evidence for divergent selection on short stamens between high and low elevations. Finally, we identified loci associated with short stamens in northeast Spain that are different from loci associated with variation in short stamens across latitudes from a previous study. Overall, we did not identify the evolutionary mechanisms contributing to an elevational cline in short stamen number so further research is clearly warranted.more » « less
-
Abstract Theory predicts that threatened species living in small populations will experience high levels of inbreeding that will increase their genetic load, but recent work suggests that the impact of load may be minimized by purging resulting from long‐term population bottlenecks. Empirical studies that examine this idea using genome‐wide estimates of inbreeding and genetic load in threatened species are limited. Here we use individual genome resequencing data to compare levels of inbreeding, levels of genetic load (estimated as mutation load) and population history in threatened Eastern massasauga rattlesnakes (Sistrurus catenatus), which exist in small isolated populations, and closely related yet outbred Western massasauga rattlesnakes (Sistrurus tergeminus). In terms of inbreeding,S. catenatusgenomes had a greater number of runs of homozygosity of varying sizes, indicating sustained inbreeding through repeated bottlenecks when compared toS. tergeminus. At the species level, outbredS. tergeminushad higher genome‐wide levels of mutation load in the form of greater numbers of derived deleterious mutations compared toS. catenatus, presumably due to long‐term purging of deleterious mutations inS. catenatus. In contrast, mutations that escaped species‐level drift effects withinS. catenatuspopulations were in general more frequent and more often found in homozygous genotypes than inS. tergeminus, suggesting a reduced efficiency of purifying selection in smallerS. catenatuspopulations for most mutations. Our results support an emerging idea that the historical demography of a threatened species has a significant impact on the type of genetic load present, which impacts implementation of conservation actions such as genetic rescue.more » « less
-
Abstract Introduced and invasive species make excellent natural experiments for investigating rapid evolution. Here, we describe the effects of genetic drift and rapid genetic adaptation in pink salmon (Oncorhynchus gorbuscha) that were accidentally introduced to the Great Lakes via a single introduction event 31 generations ago. Using whole‐genome resequencing for 134 fish spanning five sample groups across the native and introduced range, we estimate that the source population's effective population size was 146,886 at the time of introduction, whereas the founding population's effective population size was just 72—a 2040‐fold decrease. As expected with a severe founder event, we show reductions in genome‐wide measures of genetic diversity, specifically a 37.7% reduction in the number of SNPs and an 8.2% reduction in observed heterozygosity. Despite this decline in genetic diversity, we provide evidence for putative selection at 47 loci across multiple chromosomes in the introduced populations, including missense variants in genes associated with circadian rhythm, immunological response and maturation, which match expected or known phenotypic changes in the Great Lakes. For one of these genes, we use a species‐specific agent‐based model to rule out genetic drift and conclude our results support a strong response to selection occurring in a period gene (per2) that plays a predominant role in determining an organism's daily clock, matching large day length differences experienced by introduced salmon during important phenological periods. Together, these results inform how populations might evolve rapidly to new environments, even with a small pool of standing genetic variation.more » « less
An official website of the United States government
