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Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality.

ABSTRACT: Evolutionary diversification can occur in allopatry or sympatry, can be driven by selection or unselected, and can be phenotypically manifested immediately or remain latent until manifested in a newly encountered environment. Diversification of host-parasite interactions is frequently studied in the context of intrinsically selective coevolution, but the potential for host-parasite interaction phenotypes to diversify latently during parasite-blind host evolution is rarely considered. Here, we use a social bacterium experimentally adapted to several environments in the absence of phage to analyse allopatric diversification of host quality-the degree to which a host population supports a viral epidemic. Phage-blind evolution reduced host quality overall, with some bacteria becoming completely resistant to growth suppression by phage. Selective-environment differences generated only mild divergence in host quality. However, selective environments nonetheless played a major role in shaping evolution by determining the degree of stochastic diversification among replicate populations within treatments. Ancestral motility genotype was also found to strongly shape patterns of latent host-quality evolution and diversification. These outcomes show that (i) adaptive landscapes can differ in how they constrain stochastic diversification of a latent phenotype and (ii) major effects of selection on biological diversification can be missed by focusing on trait means. Collectively, our findings suggest that latent-phenotype evolution should inform host-parasite evolution theory and that diversification should be conceived broadly to include latent phenotypes.

SUBMITTER: Freund L

PROVIDER: S-EPMC8080016 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality.

Freund Lisa L Vasse Marie M Velicer Gregory J GJ

Proceedings. Biological sciences 20210428 1949

Evolutionary diversification can occur in allopatry or sympatry, can be driven by selection or unselected, and can be phenotypically manifested immediately or remain latent until manifested in a newly encountered environment. Diversification of host-parasite interactions is frequently studied in the context of intrinsically selective coevolution, but the potential for host-parasite interaction phenotypes to diversify latently during parasite-blind host evolution is rarely considered. Here, we us ...[more]

PMID: 33906400

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Project description:BackgroundEvolution in one selective environment often latently generates phenotypic change that is manifested only later in different environments, but the complexity of behavior important to fitness in the original environment might influence the character of such latent-phenotype evolution. Using Myxococcus xanthus, a bacterium possessing two motility systems differing in effectiveness on hard vs. soft surfaces, we test (i) whether and how evolution while swarming on one surface-the selective surface-latently alters motility on the alternative surface type and (ii) whether patterns of such latent-phenotype evolution depend on the complexity of ancestral motility, specific ancestral motility genotypes and/or the selective surface of evolution. We analysze an experiment in which populations established from three ancestral genotypes-one with both motility systems intact and two others with one system debilitated-evolved while swarming across either hard or soft agar in six evolutionary treatments. We then compare motility-phenotype patterns across selective vs. alternative surface types.ResultsLatent motility evolution was pervasive but varied in character as a function of the presence of one or two functional motility systems and, for some individual-treatment comparisons, the specific ancestral genotype and/or selective surface. Swarming rates on alternative vs. selective surfaces were positively correlated generally among populations with one functional motility system but not among those with two. This suggests that opportunities for pleiotropy and epistasis generated by increased genetic complexity underlying behavior can alter the character of latent-phenotype evolution. No tradeoff between motility performance across surface types was detected in the dual-system treatments, even after adaptation on a surface on which one motility system dominates strongly over the other in driving movement, but latent-phenotype evolution was instead idiosyncratic in these treatments. We further find that the magnitude of stochastic diversification at alternative-surface swarming among replicate populations greatly exceeded diversification of selective-surface swarming within some treatments and varied across treatments.ConclusionCollectively, our results suggest that increases in the genetic and mechanistic complexity of behavior can increase the complexity of latent-phenotype evolution outcomes and illustrate that diversification manifested during evolution in one environment can be augmented greatly by diversification of latent phenotypes manifested later.

Project description:RNA viruses are infamous for their high rates of mutation, which produce swarms of genetic variants within individual hosts. To date, analyses of intrahost genetic diversity have focused on the primary genome sequence. However, virus phenotypes are shaped not only by primary sequence but also by the secondary structures into which this sequence folds. Such structures enable viral replication, translation, and binding of small RNAs, yet within-host variation at the structural level has not been adequately explored. We characterized the structural diversity of the 5' untranslated region (UTR) of populations of West Nile virus (WNV) that had been subject to five serial passages in triplicate in each of three bird species. Viral genomes were sampled from host serum samples at each passage (n = 45 populations) and subjected to next-generation sequencing. For populations derived from passages 1, 3, and 5 (n = 9 populations), we predicted the impact of each mutation occurring at a frequency of ≥1% on the secondary structure of the 5' UTR. As expected, mutations in double-stranded (DS) regions of the 5' UTR stem structures caused structural changes of significantly greater magnitude than did mutations in single-stranded (SS) regions. Despite the greater impact of mutations in DS regions, mutations in DS and SS regions occurred at similar frequencies, with no evidence of enhanced selection against mutation in DS regions. In contrast, mutations in two regions that mediate genome cyclization and thereby regulate replication and translation, the 5' cyclization sequence and the UAR flanking stem (UFS), were suppressed in all three hosts.IMPORTANCE The enzymes that copy RNA genomes lack proofreading, and viruses that possess RNA genomes, such as West Nile virus, rapidly diversify into swarms of mutant lineages within a host. Intrahost variation of the primary genomic sequence of RNA viruses has been studied extensively because the extent of this variation shapes key virus phenotypes. However, RNA genomes also form complex secondary structures based on within-genome nucleotide complementarity, which are critical regulators of the cyclization of the virus genome that is necessary for efficient replication and translation. We sought to characterize variation in these secondary structures within populations of West Nile virus during serial passage in three bird species. Our study indicates that the intrahost population of West Nile virus is a diverse assortment of RNA secondary structures that should be considered in future analyses of intrahost viral diversity, but some regions that are critical for genome cyclization are conserved within hosts. Besides potential impacts on viral replication, structural diversity can influence the efficacy of small RNA antiviral therapies.

Project description:World-wide, infectious diseases represent a major source of mortality in humans and livestock. For wildlife populations, disease-induced mortality is likely even greater, but remains notoriously difficult to estimate-especially for endemic infections. Approaches for quantifying wildlife mortality due to endemic infections have historically been limited by an inability to directly observe wildlife mortality in nature. Here we address a question that can rarely be answered for endemic pathogens of wildlife: what are the population- and landscape-level effects of infection on host mortality? We combined laboratory experiments, extensive field data and novel mathematical models to indirectly estimate the magnitude of mortality induced by an endemic, virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian populations spanning four native species. We developed a flexible statistical model that uses patterns of aggregation in parasite abundance to infer host mortality. Our model improves on previous approaches for inferring host mortality from parasite abundance data by (i) relaxing restrictive assumptions on the timing of host mortality and sampling, (ii) placing all mortality inference within a Bayesian framework to better quantify uncertainty and (iii) accommodating data from laboratory experiments and field sampling to allow for estimates and comparisons of mortality within and among host populations. Applying our approach to 301 amphibian populations, we found that trematode infection was associated with an average of between 13% and 40% population-level mortality. For three of the four amphibian species, our models predicted that some populations experienced >90% mortality due to infection, leading to mortality of thousands of amphibian larvae within a pond. At the landscape scale, the total number of amphibians predicted to succumb to infection was driven by a few high mortality sites, with fewer than 20% of sites contributing to greater than 80% of amphibian mortality on the landscape. The mortality estimates in this study provide a rare glimpse into the magnitude of effects that endemic parasites can have on wildlife populations and our theoretical framework for indirectly inferring parasite-induced mortality can be applied to other host-parasite systems to help reveal the hidden death toll of pathogens on wildlife hosts.

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Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality.

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Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality.

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