Dataset Information

Approximate Bayesian estimation of coevolutionary arms races.

ABSTRACT: Exaggerated traits involved in species interactions have long captivated the imagination of evolutionary biologists and inspired the durable metaphor of the coevolutionary arms race. Despite decades of research, however, we have only a handful of examples where reciprocal coevolutionary change has been rigorously established as the cause of trait exaggeration. Support for a coevolutionary mechanism remains elusive because we lack generally applicable tools for quantifying the intensity of coevolutionary selection. Here we develop an approximate Bayesian computation (ABC) approach for estimating the intensity of coevolutionary selection using population mean phenotypes of traits mediating interspecific interactions. Our approach relaxes important assumptions of a previous maximum likelihood approach by allowing gene flow among populations, variable abiotic environments, and strong coevolutionary selection. Using simulated data, we show that our ABC method accurately infers the strength of coevolutionary selection if reliable estimates are available for key background parameters and ten or more populations are sampled. Applying our approach to the putative arms race between the plant Camellia japonica and its seed predatory weevil, Curculio camelliae, provides support for a coevolutionary hypothesis but fails to preclude the possibility of unilateral evolution. Comparing independently estimated selection gradients acting on Camellia pericarp thickness with values simulated by our model reveals a correlation between predicted and observed selection gradients of 0.941. The strong agreement between predicted and observed selection gradients validates our method.

SUBMITTER: Nuismer SL

PROVIDER: S-EPMC6483265 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Publications

Approximate Bayesian estimation of coevolutionary arms races.

Nuismer Scott L SL Week Bob B

PLoS computational biology 20190415 4

Exaggerated traits involved in species interactions have long captivated the imagination of evolutionary biologists and inspired the durable metaphor of the coevolutionary arms race. Despite decades of research, however, we have only a handful of examples where reciprocal coevolutionary change has been rigorously established as the cause of trait exaggeration. Support for a coevolutionary mechanism remains elusive because we lack generally applicable tools for quantifying the intensity of coevol ...[more]

PMID: 30986245

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Project description:BACKGROUND: The genomes of pathogens are thought to have evolved under selective pressure provided by the host in a coevolutionary arms race (the 'Red Queen's Hypothesis'). Traditionally, adaptation by pathogens is thought to rely not on whole chromosome dynamics but on gain/loss of specific genes, yielding differential abilities to infect distinct tissues. Thus, it is not known whether distinct host organs differently shape the genome of the same pathogen. We tested this hypothesis using Chlamydia trachomatis as model species, looking at 15 serovars that infect different organs: eyes, genitalia and lymph nodes. RESULTS: We analyzed over 51,000 base pairs from all serovars using various phylogenetic approaches and a non-phylogenetic indel-based algorithm to study the evolution of individual and concatenated loci. This survey comprised about 33% of all single nucleotide polymorphisms in C. trachomatis chromosomes. We present a model in which genome evolution indeed correlates with the cell type (epithelial versus lymph cells) and organ (eyes versus genitalia) that a serovar infects, illustrating an adaptation to physiologically distinct niches, and discarding genetic drift as the dominant evolutionary driving force. We show that radiation of serovars occurred primarily by accumulation of single nucleotide polymorphisms in intergenomic regions, housekeeping genes, and genes encoding hypothetical and cell envelope proteins. Furthermore, serovar evolution also correlates with ecological success, as the two most successful serovars showed a parallel evolution. CONCLUSION: We identified a single nucleotide polymorphism-based tissue-specific arms race for strains in the same species, reflecting global chromosomal dynamics. Studying such tissue-specific arms race scenarios is crucial for understanding pathogen-host interactions during the course of infectious diseases, in order to dissect pathogen biology and develop preventive and therapeutic strategies.

Project description:Viral receptors are the cell surface proteins that are hijacked by viruses to initialize their infections. Viral receptors are subject to two conflicting directional forces, namely, negative selection due to functional constraints and positive selection due to host-virus arms races. It remains largely obscure whether negative pleiotropy limits the rate of adaptation in viral receptors. Here, we perform evolutionary analyses of 96 viral receptor genes in primates and find that 41 out of 96 viral receptors experienced adaptive evolution. Many positively selected residues in viral receptors are located at the virus-receptor interfaces. Compared with control proteins, viral receptors exhibit significantly elevated rate of adaptation. Further analyses of genetic polymorphisms in human populations reveal signals of positive selection and balancing selection for 53 and 5 viral receptors, respectively. Moreover, we find that 49 viral receptors experienced different selection pressures in different human populations, indicating that viruses represent an important driver of local adaptation in humans. Our findings suggest that diverse viruses, many of which have not been known to infect nonhuman primates, have maintained antagonistic associations with primates for millions of years, and the host-virus conflicts drive accelerated adaptive evolution in viral receptors.IMPORTANCE Viruses hijack cellular proteins, termed viral receptors, to assist their entry into host cells. While viral receptors experience negative selection to maintain their normal functions, they also undergo positive selection due to an everlasting evolutionary arms race between viruses and hosts. A complete picture on how viral receptors evolve under two conflicting forces is still lacking. In this study, we systematically analyzed the evolution of 96 viral receptors in primates and human populations. We found around half of viral receptors underwent adaptive evolution and exhibit significantly elevated rates of adaptation compared to control genes in primates. We also found signals of past natural selection for 58 viral receptors in human populations. Interestingly, 49 viral receptors experienced different selection pressures in different human populations, indicating that viruses represent an important driver of local adaptation in humans. Our results suggest that host-virus arms races drive accelerated adaptive evolution in viral receptors.

Dataset Information

Approximate Bayesian estimation of coevolutionary arms races.

Publications

Approximate Bayesian estimation of coevolutionary arms races.

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