Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts

South African National Bioinformatics Institute, University of the Western Cape, Cape Town, South Africa.
Virology Journal (Impact Factor: 2.18). 02/2009; 6(1):104. DOI: 10.1186/1743-422X-6-104
Source: PubMed


Despite the demonstration that geminiviruses, like many other single stranded DNA viruses, are evolving at rates similar to those of RNA viruses, a recent study has suggested that grass-infecting species in the genus Mastrevirus may have co-diverged with their hosts over millions of years. This "co-divergence hypothesis" requires that long-term mastrevirus substitution rates be at least 100,000-fold lower than their basal mutation rates and 10,000-fold lower than their observable short-term substitution rates. The credibility of this hypothesis, therefore, hinges on the testable claim that negative selection during mastrevirus evolution is so potent that it effectively purges 99.999% of all mutations that occur.
We have conducted long-term evolution experiments lasting between 6 and 32 years, where we have determined substitution rates of between 2 and 3 x 10(-4) substitutions/site/year for the mastreviruses Maize streak virus (MSV) and Sugarcane streak Réunion virus (SSRV). We further show that mutation biases are similar for different geminivirus genera, suggesting that mutational processes that drive high basal mutation rates are conserved across the family. Rather than displaying signs of extremely severe negative selection as implied by the co-divergence hypothesis, our evolution experiments indicate that MSV and SSRV are predominantly evolving under neutral genetic drift.
The absence of strong negative selection signals within our evolution experiments and the uniformly high geminivirus substitution rates that we and others have reported suggest that mastreviruses cannot have co-diverged with their hosts.

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Available from: Darren P Martin, Oct 06, 2015
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    • "Bernard 1994; Pavesi 2005; Gibbs et al. 2010; Torres-P erez et al. 2011). However, for fast evolving viruses, such as those with RNA or small, single-stranded (ss) DNA genomes, the temporal scales of host and virus evolution may be broadly different (Duffy & Holmes 2008; Holmes 2009; Lefeuvre et al. 2011), and codivergence has most often not been observed, or reported examples have been challenged (Harkins et al. 2009; Holmes 2009). Importantly , most studies have focused on demonstrating codivergence at an interspecific rather than at the interpopulation level and mainly neglect which ecological factors drive this process (Paterson & Piertney 2011; but see Torres-P erez et al. 2011). "
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    ABSTRACT: Knowledge on how landscape heterogeneity shapes host-parasite interactions is central to understand the emergence, dynamics and evolution of infectious diseases. However, this is an underexplored subject, particularly for plant-virus systems. Here, we analyse how landscape heterogeneity influences the prevalence, spatial genetic structure, and temporal dynamics of Pepper golden mosaic and Pepper huasteco yellow vein begomoviruses infecting populations of the wild pepper Capsicum annuum glabriusculum (chiltepin) in Mexico. Environmental heterogeneity occurred at different nested spatial scales (host populations within biogeographical provinces), with levels of human management varying among host population within a province. Results indicate that landscape heterogeneity affects the epidemiology and genetic structure of chiltepin-infecting begomoviruses in a scale-specific manner, probably related to conditions favouring the viruses' whitefly vector and its dispersion. Increased levels of human management of the host populations were associated with higher virus prevalence and erased the spatial genetic structure of the virus populations. Also, environmental heterogeneity similarly shaped the spatial genetic structures of host and viruses. This resulted in the congruence between host and virus phylogenies, which does not seem to be due to host-virus co-evolution. Thus, results provide evidence of the key role of landscape heterogeneity in determining plant-virus interactions.
    Molecular Ecology 02/2013; 22(8). DOI:10.1111/mec.12232 · 6.49 Impact Factor
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    • "For the recombinant MSV data we detected the same imbalance between G → T : C → A mutations (8:2 mutations; p = 0.132) as has been detected previously in long-term evolution experiments involving MSV [18,29], and the mastrevirus Sugarcane streak Reunion virus (SSRV [18]; Table 1). Importantly, when the mutations from the recombinant MSV data, VWMPCPLIRMat and wt isolates (MSV-MatA and MSV-VW) were combined with those obtained previously in evolution experiments involving the field isolates MSV-Tas, MSV-Set and MSV-Kom and MSV-Kom/Set chimaeric viruses [29], further imbalances in G → T : C → A (29:9 mutations; p = 0.004), G → A : C → T (18:30 mutations; p = 0.052), and A → G : T → C (16:6 mutations; p = 0.054) were detected. "
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    ABSTRACT: Background Single-stranded (ss) DNA viruses in the family Geminiviridae are proving to be very useful in real-time evolution studies. The high mutation rate of geminiviruses and other ssDNA viruses is somewhat mysterious in that their DNA genomes are replicated in host nuclei by high fidelity host polymerases. Although strand specific mutation biases observed in virus species from the geminivirus genus Mastrevirus indicate that the high mutation rates in viruses in this genus may be due to mutational processes that operate specifically on ssDNA, it is currently unknown whether viruses from other genera display similar strand specific mutation biases. Also, geminivirus genomes frequently recombine with one another and an alternative cause of their high mutation rates could be that the recombination process is either directly mutagenic or produces a selective environment in which the survival of mutants is favoured. To investigate whether there is an association between recombination and increased basal mutation rates or increased degrees of selection favoring the survival of mutations, we compared the mutation dynamics of the MSV-MatA and MSV-VW field isolates of Maize streak virus (MSV; Mastrevirus), with both a laboratory constructed MSV recombinant, and MSV recombinants closely resembling MSV-MatA. To determine whether strand specific mutation biases are a general characteristic of geminivirus evolution we compared mutation spectra arising during these MSV experiments with those arising during similar experiments involving the geminivirus Tomato yellow leaf curl virus (Begomovirus genus). Results Although both the genomic distribution of mutations and the occurrence of various convergent mutations at specific genomic sites indicated that either mutation hotspots or selection for adaptive mutations might elevate observed mutation rates in MSV, we found no association between recombination and mutation rates. Importantly, when comparing the mutation spectra of MSV and TYLCV we observed similar strand specific mutation biases arising predominantly from imbalances in the complementary mutations G → T: C → A. Conclusions While our results suggest that recombination does not strongly influence mutation rates in MSV, they indicate that high geminivirus mutation rates are at least partially attributable to increased susceptibility of all geminivirus genomes to oxidative damage while in a single stranded state.
    BMC Evolutionary Biology 12/2012; 12(1):252. DOI:10.1186/1471-2148-12-252 · 3.37 Impact Factor
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    • "Instead of changing many dates of isolation, however, only AY269825 would have to be assigned a different date (removing the four taxa that grouped with AY269825 did not change the estimated substitution rate or TMRCA of RHDV, data not shown). Previous studies have shown that the long-term rate of viral evolution in the lab can mimic the rate in nature [52], so unlike the 20 years of frozen stasis that the Influenza isolate experienced, AY269825 was changing at a rate similar to its wild relatives. "
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    ABSTRACT: The literature is ripe with phylogenetic estimates of nucleotide substitution rates, especially of measurably evolving species such as RNA viruses. However, it is not known how robust these rate estimates are to inaccuracies in the data, particularly in sampling dates that are used for molecular clock calibration. Here we report on the rate of evolution of the emerging pathogen Rabbit hemorrhagic disease virus (RHDV), which has significantly different rates of evolution for the same outer capsid (VP60) gene published in the literature. In an attempt to reconcile the conflicting data and further elucidate details of RHDV 's evolutionary history, we undertook fresh Bayesian analyses and employed jackknife control methods to produce robust substitution rate and time to most recent common ancestor (TMRCA) estimates for RHDV based on the VP60 and RNA-dependent RNA polymerase genes. Through these control methods, we were able to identify a single misdated taxon, a passaged lab strain used for vaccine production, which was responsible for depressing the RHDV capsid gene's rate of evolution by 65%. Without this isolate, the polymerase and the capsid protein genes had nearly identical rates of evolution: 1.90x10-3 nucleotide substitutions/site/year, ns/s/y, (95% highest probability density (HPD) 1.25x10-3-2.55x10-3) and 1.91x10-3 ns/s/y (95% HPD 1.50x10-3-2.34x10-3), respectively. After excluding the misdated taxon, both genes support a significantly higher substitution rate as well as a relatively recent emergence of RHDV, and obviate the need for previously hypothesized decades of unobserved diversification of the virus. The control methods show that using even one misdated taxon in a large dataset can significantly skew estimates of evolutionary parameters and suggest that it is better practice to use smaller datasets composed of taxa with unequivocal isolation dates. These jackknife controls would be useful for future tip-calibrated rate analyses that include taxa with ambiguous dates of isolation.
    BMC Evolutionary Biology 05/2012; 12(1):74. DOI:10.1186/1471-2148-12-74 · 3.37 Impact Factor
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