Drift rather than host or parasite control can explain within-host Wolbachia growth
Wolbachia load variation in Drosophila is more likely caused by drift than by host genetic factors
Recommendation: posted 04 May 2021, validated 11 May 2021
Within-host parasite density is tightly linked to parasite fitness often determining both transmission success and virulence (parasite-induced harm to the host) (Alizon et al., 2009, Anderson & May, 1982). Parasite density may thus be controlled by selection balancing these conflicting pressures. Actual within-host density regulation may be under host or parasite control, or due to other environmental factors (Wale et al., 2019, Vale et al., 2011, Chrostek et al., 2013). Vertically transmitted parasites may also be more vulnerable to drift associated with bottlenecks between generations, which may also determine within-host population size (Mathe-Hubert et al., 2019, Mira & Moran, 2002).
Bénard et al. (2021) use 3 experiments to disentangle the role of drift versus host factors in the control of within-host Wolbachia growth in Drosophila melanogaster. They use the wMelPop Wolbachia strain in which virulence (fly longevity) and within-host growth correlate positively with copy number in the genomic region Octomom (Chrostek et al., 2013, Chrostek & Teixeira, 2015). Octomom copy number can be used as a marker for different genetic lineages within the wMelPop strain.
In a first experiment, they introgressed and backcrossed this Wolbachia strain into 6 different host genetic backgrounds and show striking differences in within-host symbiont densities which correlate positively with Octomom copy number. This is consistent with host genotype selecting different Wolbachia strains, but also with bottlenecks and drift between generations. To distinguish between these possibilities, they perform 2 further experiments.
A second experiment repeated experiment 1, but this time introgression was into 3 independent lines of the Bolivia and USA Drosophila populations; those that, respectively, exhibited the lowest and highest Wolbachia density and Octomom copy number. In this experiment, growth and Octomom copy number were measured across the 3 lines, for each population, after 1, 13 and 25 generations. Although there were little differences between replicates at generation 1, there were differences at generations 13 and 25 among the replicates of both the Bolivia and USA lines. These results are indicative of parasite control, or drift being responsible for within-host growth rather than host factors.
A third experiment tested whether Wolbachia density and copy number were under host or parasite control. This was done, again using the USA and Bolivia lines, but this time those from the first experiment, several generations following the initial introgression and backcrossing. The newly introgressed lines were again followed for 25 generations. At generation 1, Wolbachia phenotypes resembled those of the donor parasite population and not the recipient host population indicating a possible maternal effect, but a lack of host control over the parasite. Furthermore, Wolbachia densities and Octomom number differed among replicate lines through time for Bolivia populations and from the donor parasite lines for both populations. These differences among replicate lines that share both host and parasite origins suggest that drift and/or maternal effects are responsible for within-host Wolbachia density and Octomom number.
These findings indicate that drift appears to play a role in shaping Wolbachia evolution in this system. Nevertheless, completely ruling out the role of the host or parasite in controlling densities will require further study. The findings of Bénard and coworkers (2021) should stimulate future work on the contribution of drift to the evolution of vertically transmitted parasites.
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Alison Duncan and Michael Hochberg (2021) Drift rather than host or parasite control can explain within-host Wolbachia growth. Peer Community in Evolutionary Biology, 100126. 10.24072/pci.evolbiol.100126
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
Evaluation round #2
DOI or URL of the preprint: https://doi.org/10.1101/2020.11.29.402545
Version of the preprint: https://www.biorxiv.org/content/10.1101/2020.11.29.402545v2
Author's Reply, 04 May 2021
Decision by Michael Hochberg and Alison Duncan, posted 16 Apr 2021
The two reviewers were satisfied overall with your revisions and recommend that following these your preprint be approved by PCI. In parallel, Dr. Alison Duncan, who is co-recommending your preprint, has made numerous minor corrections to the manuscript that we hope you will consider in your revised submission. I will send the Word doc to you shortly.
MichaelDownload recommender's annotations
Reviewed by Simon Fellous, 22 Mar 2021
Reviewed by anonymous reviewer, 14 Apr 2021
Evaluation round #1
DOI or URL of the preprint: 10.1101/2020.11.29.402545
Author's Reply, 17 Mar 2021
Decision by Michael Hochberg and Alison Duncan, posted 21 Jan 2021
Dear Dr. Kremer,
Your preprint has now been seen by two Reviewers. Their comments accompany this letter. Although both see interest in what your study attempts to achieve, they both have major reservations about the interpretation of the results. Both Reviewers question whether the study convincingly shows drift (and the absence of host genotype effects). Their arguments about possible alternative explanations for your results suggest that you will need to rethink your interpretations and revise accordingly, with the possible additional presentations/analyses suggested notably by Reviewer 2.
I would therefore encourage you to revise and resubmit your preprint to PCI Evolutionary Biology together with point-by-point replies to each of the reviewers’ comments. Please indicate in each reply where changes were made in the manuscript. Once your revision is received, we will contact both reviewers for their views on whether their concerns have been adequately addressed.
Yours sincerely, Michael Hochberg