Two modes of evolution shape bacterial strain diversity in the gut for thousands of generations

How and at what pace bacteria evolve when colonizing healthy hosts remains unclear. Here, by monitoring evolution for more than six thousand generations in the mouse gut, we show that the successful colonization of an invader Escherichia coli depends on the diversity of the existing microbiota and the presence of a closely related strain. Following colonization, two modes of evolution were observed: one in which diversifying selection leads to long-term coexistence of ecotypes and a second in which directional selection propels selective sweeps. These modes can be quantitatively distinguished by the statistics of mutation trajectories. In our experiments, diversifying selection was marked by the emergence of metabolic mutations, and directional selection by acquisition of prophages, which bring their own benefits and costs. In both modes, we observed parallel evolution, with mutation accumulation rates comparable to those typically observed in vitro on similar time scales. Our results show that gut environments can rapidly generate diversifying selection and ecotype formation.

Defensive Symbionts and the Evolution of Parasitoid Host Specialization

Insect host–parasitoid interactions abound in nature and are characterized by a high degree of host specialization. In addition to their behavioral and immune defenses, many host species rely on heritable bacterial endosymbionts for defense against parasitoids. Studies on aphids and flies show that resistance conferred by symbionts can be very strong and highly specific, possibly as a result of variation in symbiont-produced toxins. I argue that defensive symbionts are therefore an important source of diversifying selection, promoting the evolution of host specialization by parasitoids. This is likely to affect the structure of host–parasitoid food webs. I consider potential changes in terms of food web complexity, although the nature of these effects will also be influenced by whether maternally transmitted symbionts have some capacity for lateral transfer. This is discussed in the light of available evidence for horizontal transmission routes. Finally, I propose that defensive mutualisms other than microbial endosymbionts may also exert diversifying selection on insect parasitoids. Expected final online publication date for the Annual Review of Entomology, Volume 67 is January 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Multiple Mechanisms Drive the Evolutionary Adaptation of Phytophthora infestans Effector Avr1 to Host Resistance

Effectors, a group of small proteins secreted by pathogens, play a central role in antagonistic interactions between plant hosts and pathogens. The evolution of effector genes threatens plant disease management and sustainable food production, but population genetic analyses to understand evolutionary mechanisms of effector genes are limited compared to molecular and functional studies. Here we investigated the evolution of the Avr1 effector gene from 111 Phytophthora infestans isolates collected from six areas covering three potato cropping regions in China using a population genetic approach. High genetic variation of the effector gene resulted from diverse mechanisms including base substitution, pre-termination, intragenic recombination and diversifying selection. Nearly 80% of the 111 sequences had a point mutation in the 512th nucleotide (T512G), which generated a pre-termination stop codon truncating 38 amino acids in the C-terminal, suggesting that the C-terminal may not be essential to ecological and biological functions of P. infestans. A significant correlation between the frequency of Avr1 sequences with the pre-termination and annual mean temperature in the collection sites suggests that thermal heterogeneity might be one of contributors to the diversifying selection, although biological and biochemical mechanisms of the likely thermal adaptation are not known currently. Our results highlight the risk of rapid adaptation of P. infestans and possibly other pathogens as well to host resistance, and the application of eco-evolutionary principles is necessary for sustainable disease management in agricultural ecosystems.

RV144 Vaccine Imprinting Constrained HIV-1 Evolution Following Breakthrough Infection

The scale of the HIV-1 epidemic underscores the need for a vaccine. The multitude of circulating HIV-1 strains together with HIV-1’s high evolvability hint that HIV-1 could adapt to a future vaccine. Here we wanted to investigate the effect of vaccination on the evolution of the virus post-breakthrough infection. We analyzed 2,635 HIV-1 env sequences sampled up to a year post-diagnosis from 110 vaccine and placebo participants who became infected in the RV144 vaccine efficacy trial. We showed that the Env signatures sites that were previously identified to distinguish vaccine and placebo participants were maintained over time. In addition, fewer sites were under diversifying selection in the vaccine group than in the placebo group. These results indicate that HIV-1 would possibly adapt to a vaccine upon its roll out.

The Genetic Variation Landscape of African Swine Fever Virus Reveals Frequent Positive Selection on Amino Acid Replacements

African swine fever virus (ASFV) is a lethal disease agent that causes high mortality in swine population and devastating loss in swine industries. The development of efficacious vaccines has been hindered by the knowledge gap in genetic properties of ASFV and the interface of virus-host interactions. In this study, we performed a genetic study of ASFV aiming to profile the variation landscape and identify genetic factors with signatures of positive selection and relevance to virus-host interactions. To achieve this goal, we developed a new tool “SweepCluster” for systematic identification of selective sweep. Our data reveals a high level of genetic variability of ASFV shaped by both diversifying selection and selective sweep. The selection signatures are widely distributed across the genome with the diversifying selection falling within 29 genes and selection sweep within 25 genes. Further examination of the structure properties reveals the link of the selection signatures with virus-host interactions. Specifically, we discovered a site at 157th of the antigen protein EP402R under diversifying selection located in the cytotoxic T-cell epitope involved in the serotype-specific T-cell response. Moreover, we reported 24 novel candidate genes with relevance to virus-host interactions. By integrating the candidate genes with selection signatures into a unified framework of interactions between ASFV and hosts, we showed that those genes are involved in multiple processes of host immune evasion and virus life cycles, and may play crucial roles in circumventing host defense systems and enhancing adaptive fitness.ImportanceASFV causes lethal disease in swine population with up to 100% mortality rates in domestic pigs. The recent outbreak of the disease has spread rapidly worldwide resulting in a large amount of deaths of pigs and tremendous damages to the swine industry. There is no commercially available vaccine against ASFV infection. Current vaccine strategies face the challenges of incomplete protection or deficient cross-protection. The challenges strongly highlight the need for thorough understanding of genetic properties at the interface of virus-host interactions. In this study, we developed a new bioinformatics tool “SweepCluster” and employed computational approaches to characterize the genetic variation landscape of the virus aiming to identify genetic factors relevant to host interactions. The results we present will allow enhanced understanding of genetic basis of rapid adaptation of ASFV and provide valuable targets for therapeutic intervention. The new analytic tool we offer could be used as a general approach for selection analysis.

Adaptive Molecular Evolution of AKT3 Gene for Positive Diversifying Selection in Mammals

The V-Akt Murine Thymoma Viral Oncogene Homolog 3 (AKT3) gene is of the serine/threonine-protein kinase family and influences the production of milk fats and cholesterol by acting on the sterol administrative area restricting protein (SREBP). The AKT3 gene is highly preserved in animals, and during lactation in cattle, its expression increases. The AKT3 gene is expressed in the digestive system, mammary gland, and immune cells. A phylogenetic investigation was performed to clarify the evolutionary role of AKT3, by maximum probability. The AKT3 gene sequence data of various mammalian species was evident even with animals undergoing breeding selection. From 39 mammalian species studied, there was a signal of positive diversifying selection with Hominidae at 13Q, 16G, 23R, 24P, 121P, 294K, 327V, 376L, 397K, 445T, and 471F among other codon sites of the AKT3 gene. These sites were codes for amino acids such as arginine, proline, lysine, and leucine indicating major roles for the function of immunological proteins, and in particular, the study highlighted the importance of changes in gene expression of AKT3 on immunity.