Effects of periodic bottlenecks on the dynamics of adaptive evolution in microbial populations

Population bottlenecks are common in nature, and they can impact the rate of adaptation in evolving populations. On the one hand, each bottleneck reduces the genetic variation that fuels adaptation. On the other hand, fewer founders can undergo more generations and leave more descendants in a resource-limited environment, which allows surviving beneficial mutations to spread more quickly. Here we investigate the impact of repeated bottlenecks on the dynamics of adaptation in experimental populations of Escherichia coli. We propagated 48 populations under four dilution regimes (2-, 8-, 100-, and 1000-fold), all reaching the same final size each day, for 150 days. A simple model in which adaptation is limited by the supply rate of beneficial mutations predicts that fitness gains should be maximized with ~8-fold dilutions. The model also assumes that selection acts only on the overall growth rate and is otherwise identical across dilution regimes. However, we found that selection in the 2-fold regime was qualitatively different from the other treatments. Moreover, we observed earlier and greater fitness gains in the populations subjected to 100- and 1000-fold dilutions than in those that evolved in the 8 fold regime. We also ran simulations using parameters estimated independently from a long-term experiment using the same ancestral strain and environment. The simulations produced dynamics similar to our empirical results under these regimes, and they indicate that the simple model fails owing to the assumption that the supply of beneficial mutations limits adaptation.

Genomic epidemiological models describe pathogen evolution across fitness valleys

Genomics is fundamentally changing epidemiological research. However, exploring hypotheses about pathogen evolution in different epidemiological contexts poses new challenges. Models intertwining pathogen epidemiology and genomic evolution can help understand processes such as the emergence of novel pathogen genotypes with higher transmission or resistance to treatment. In this work, we present Opqua, a computational framework for flexible simulation of pathogen epidemiology and evolution. We use Opqua to study determinants of evolution across fitness valleys. We confirm that competition can limit evolution in high transmission environments and find that low transmission, host mobility, and complex pathogen life cycles facilitate reaching new adaptive peaks through population bottlenecks and decoupling selective pressures. The results show the potential of genomic epidemiological modeling as a tool in infectious disease research.

Genetic Diversity and Population Dynamics of Leptobrachium leishanense (Anura: Megophryidae) as Determined by Tetranucleotide Microsatellite Markers Developed from Its Genome

Persisting declination of amphibians around the world has resulted in the public attaching importance to the conservation of their biodiversity. Genetic data can be greatly helpful in conservation planning and management, especially in species that are small in size and hard to observe. It is essential to perform genetic assessments for the conservation of Leptobrachium leishanense, an endangered toad and receiving secondary protection on the list of state-protected wildlife in China. However, current molecular markers with low reliability and efficiency hinder studies. Here, we sampled 120 adult toes from the population in the Leishan Mountain, 23 of which were used to develop tetranucleotide microsatellite markers based on one reference L. leishanense genome. After primer optimization, stability detection, and polymorphism detection, we obtained 12 satisfactory microsatellite loci. Then, we used these loci to evaluate the genetic diversity and population dynamics of the 120 individuals. Our results show that there is a low degree of inbreeding in the population, and it has a high genetic diversity. Recently, the population has not experienced population bottlenecks, and the estimated effective population size was 424.3. Accordingly, stabilizing genetic diversity will be key to population sustainability. Recovering its habitat and avoiding intentional human use will be useful for conservation of this species.

Population genomics and evidence of clonal replacement of Plasmodium falciparum in the Peruvian Amazon

Previous studies have shown that P. falciparum parasites in South America have undergone population bottlenecks resulting in clonal lineages that are differentially distributed and that have been responsible for several outbreaks different endemic regions. In this study, we explored the genomic profile of 18 P. falciparum samples collected in the Peruvian Amazon Basin (Loreto) and 6 from the Peruvian North Coast (Tumbes). Our results showed the presence of three subpopulations that matched previously typed lineages in Peru: Bv1 (n = 17), Clonet D (n = 4) and Acre-Loreto type (n = 3). Gene coverage analysis showed that none of the Bv1 samples presented coverage for pfhrp2 and pfhrp3. Genotyping of drug resistance markers showed a high prevalence of Chloroquine resistance mutations S1034C/N1042D/D1246Y in pfmdr1 (62.5%) and K45T in pfcrt (87.5%). Mutations associated with sulfadoxine and pyrimethamine treatment failure were found on 88.8% of the Bv1 samples which were triple mutants for pfdhfr (50R/51I/108N) and pfdhps (437G/540E/581G). Analysis of the pfS47 gene that allows P. falciparum to evade mosquito immune responses showed that the Bv1 lineage presented one pfS47 haplotype exclusive to Loreto and another haplotype that was present in both Loreto and Tumbes. Furthermore, a possible expansion of Bv1 was detected since 2011 in Loreto. This replacement could be a result of the high prevalence of CQ resistance polymorphisms in Bv1, which could have provided a selective advantage to the indirect selection pressures driven by the use of CQ for P. vivax treatment.

Genomic analysis of a parasite invasion: colonization of the Americas by the blood fluke, Schistosoma mansoni

Schistosoma mansoni, a snail-vectored blood fluke that infects humans, was introduced into the Americas from Africa during the Trans-Atlantic slave trade. As this parasite shows strong specificity to the snail intermediate host, we expected that adaptation to S. American Biomphalaria spp. snails would result in population bottlenecks and strong signatures of selection. We scored 475,081 single nucleotide variants (SNVs) in 143 S. mansoni from the Americas (Brazil, Guadeloupe, and Puerto Rico) and Africa (Cameroon, Niger, Senegal, Tanzania, and Uganda), and used these data to ask: (i) Was there a population bottleneck during colonization? (ii) Can we identify signatures of selection associated with colonization? And (iii) what were the source populations for colonizing parasites? We found a 2.4-2.9-fold reduction in diversity and much slower decay in linkage disequilibrium (LD) in parasites from East to West Africa. However, we observed similar nuclear diversity and LD in West Africa and Brazil, suggesting no strong bottlenecks and limited barriers to colonization. We identified five genome regions showing selection in the Americas, compared with three in West Africa and none in East Africa, which we speculate may reflect adaptation during colonization. Finally, we infer that unsampled African populations from central African regions between Benin and Angola, with contributions from Niger, are likely the major source(s) for Brazilian S. mansoni. The absence of a bottleneck suggests that this is a rare case of a serendipitous invasion, where S. mansoni parasites were preadapted to the Americas and were able to establish with relative ease.

Pseudofinder: detection of pseudogenes in prokaryotic genomes

Prokaryotic genomes are generally gene dense and encode relatively few pseudogenes, or nonfunctional/inactivated remnants of genes. However, in certain contexts, such as recent ecological shifts or extreme population bottlenecks (such as those experienced by symbionts and pathogens), pseudogenes can quickly accumulate and form a substantial fraction of the genome. Identification of pseudogenes is, thus, a critical step for understanding the evolutionary forces acting upon, and the functional potential encoded within, prokaryotic genomes. Here, we present Pseudofinder, an open-source software dedicated to pseudogene identification and analysis. With Pseudofinder's multi-pronged, reference-based approach, we demonstrate its capacity to detect a wide variety of pseudogenes, including those that are highly degraded and typically missed by gene-calling pipelines, as well newly formed pseudogenes, which can have only one or a few inactivating mutations. Additionally, Pseudofinder can detect intact genes undergoing relaxed selection, which may indicate incipient pseudogene formation. Implementation of Pseudofinder in annotation pipelines will not only clarify the functional potential of sequenced microbes, but will also generate novel insights and hypotheses regarding the evolutionary dynamics of bacterial and archaeal genomes.

Long-Term Population Dynamics of Namib Desert Tenebrionid Beetles Reveal Complex Relationships to Pulse-Reserve Conditions

Noy-Meir’s paradigm concerning desert populations being predictably tied to unpredictable productivity pulses was tested by examining abundance trends of 26 species of flightless detritivorous tenebrionid beetles (Coleoptera, Tenebrionidae) in the hyper-arid Namib Desert (MAP = 25 mm). Over 45 years, tenebrionids were continuously pitfall trapped on a gravel plain. Species were categorised according to how their populations increased after 22 effective rainfall events (>11 mm in a week), and declined with decreasing detritus reserves (97.7–0.2 g m−2), while sustained by nonrainfall moisture. Six patterns of population variation were recognised: (a) increases triggered by effective summer rainfalls, tracking detritus over time (five species, 41% abundance); (b) irrupting upon summer rainfalls, crashing a year later (three, 18%); (c) increasing gradually after series of heavy (>40 mm) rainfall years, declining over the next decade (eight, 15%); (d) triggered by winter rainfall, population fluctuating moderately (two, 20%); (e) increasing during dry years, declining during wet (one, 0.4%); (f) erratic range expansions following heavy rain (seven, 5%). All species experienced population bottlenecks during a decade of scant reserves, followed by the community cycling back to its earlier composition after 30 years. By responding selectively to alternative configurations of resources, Namib tenebrionids showed temporal patterns and magnitudes of population fluctuation more diverse than predicted by Noy-Meir’s original model, underpinning high species diversity.

Genealogical structure changes as range expansions transition from pushed to pulled

Range expansions accelerate evolution through multiple mechanisms, including gene surfing and genetic drift. The inference and control of these evolutionary processes ultimately rely on the information contained in genealogical trees. Currently, there are two opposing views on how range expansions shape genealogies. In invasion biology, expansions are typically approximated by a series of population bottlenecks producing genealogies with only pairwise mergers between lineages—a process known as the Kingman coalescent. Conversely, traveling wave models predict a coalescent with multiple mergers, known as the Bolthausen–Sznitman coalescent. Here, we unify these two approaches and show that expansions can generate an entire spectrum of coalescent topologies. Specifically, we show that tree topology is controlled by growth dynamics at the front and exhibits large differences between pulled and pushed expansions. These differences are explained by the fluctuations in the total number of descendants left by the early founders. High growth cooperativity leads to a narrow distribution of reproductive values and the Kingman coalescent. Conversely, low growth cooperativity results in a broad distribution, whose exponent controls the merger sizes in the genealogies. These broad distribution and non-Kingman tree topologies emerge due to the fluctuations in the front shape and position and do not occur in quasi-deterministic simulations. Overall, our results show that range expansions provide a robust mechanism for generating different types of multiple mergers, which could be similar to those observed in populations with strong selection or high fecundity. Thus, caution should be exercised in making inferences about the origin of non-Kingman genealogies.

Brief Population Bottlenecks Are Beyond The Genetic Streetlight

Inferring human demographic history from extant genomes is an important goal of population genetics. To date, the sensitivity of coalescence-based methods in detecting population bottlenecks has not been well characterized. In this study, we find that brief bottlenecks, of just a few generations, are undetectable by current methods. A new approach to population inference, Lineage Time Inference (LiTI), uses data-derived windows to demarcate the limits of the genetic data. We find that a sharp population bottleneck at the time of the Youngest Toba Eruption, and also at more ancient timepoints in the human lineage, would be outside the genetic streetlight.

Grape Phylloxera Genetic Structure Reveals Root–Leaf Migration within Commercial Vineyards

Depending on their life cycle, grape phylloxera (Daktulosphaira vitifoliae Fitch) leaf-feeding populations are initiated through asexually produced offspring or sexual recombination. The vine’s initial foliar larvae may originate from root-feeding phylloxera or wind-drifted foliar larvae from other habitats. Though some studies have reported phylloxera leaf-feeding in commercial vineyards, it is still unclear if they are genetically distinct from the population structure of these two sources. Using seven SSR-markers, this study analyzed the genetic structure of phylloxera populations in commercial vineyards with different natural infestation scenarios and that of single-plant insect systems that exclude infestation by wind-drifted larvae. We saw that during the vegetation period, phylloxera populations predominately go through their asexual life cycle to migrate from roots to leaves. We provided evidence that such migrations do not exclusively occur through wind-drifted foliar populations from rootstock vines in abandoned thickets, but that root populations within commercial vineyards also migrate to establish V. vinifera leaf populations. Whereas the former scenario generates foliar populations with high genotypic diversity, the latter produces population bottlenecks through founder effects or phylloxera biotype selection pressure. We finally compared these population structures with those of populations in their native habitat in North America, using four microsatellite markers.