The potential evolutionary importance of low-frequency flexibility in reproductive modes
Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?
Recommendation: posted 16 June 2022, validated 17 June 2022
Occasional events of asexual reproduction in otherwise sexual taxa have been documented since a long time. Accounts range from observations of offspring development from unfertilized eggs in Drosophila to rare offspring production by isolated females in lizards and birds (e.g., Stalker 1954, Watts et al 2006, Ryder et al. 2021). Many more such cases likely await documentation, as rare events are inherently difficult to observe. These rare events of asexual reproduction are often associated with low offspring fitness (“tychoparthenogenesis”), and have mostly been discarded in the evolutionary literature as reproductive accidents without evolutionary significance. Recently, however, there has been an increased interest in the details of evolutionary transitions from sexual to asexual reproduction (e.g., Archetti 2010, Neiman et al.2014, Lenormand et al. 2016), because these details may be key to understanding why successful transitions are rare, why they occur more frequently in some groups than in others, and why certain genetic mechanisms of ploidy maintenance or ploidy restoration are more often observed than others. In this context, the hypothesis has been formulated that regular or even obligate asexual reproduction may evolve from these rare events of asexual reproduction (e.g., Schwander et al. 2010).
A new study by Capdevielle Dulac et al. (2022) now investigates this question in a parasitoid wasp, highlighting also the fact that what is considered rare or occasional may differ from one system to the next. The results show “rare” parthenogenetic production of diploid daughters occurring at variable frequencies (from zero to 2 %) in different laboratory strains, as well as in a natural population. They also demonstrate parthenogenetic production of female offspring in both virgin females and mated ones, as well as no reduced fecundity of parthenogenetically produced offspring. These findings suggest that parthenogenetic production of daughters, while still being rare, may be a more regular and less deleterious reproductive feature in this species than in other cases of occasional asexuality. Indeed, haplodiploid organisms, such as this parasitoid wasp have been hypothesized to facilitate evolutionary transitions to asexuality (Neimann et al. 2014, Van Der Kooi et al. 2017). First, in haploidiploid organisms, females are diploid and develop from normal, fertilized eggs, but males are haploid as they develop parthenogenetically from unfertilized eggs. This means that, in these species, fertilization is not necessarily needed to trigger development, thus removing one of the constraints for transitions to obligate asexuality (Engelstädter 2008, Vorburger 2014). Second, spermatogenesis in males occurs by a modified meiosis that skips the first meiotic division (e.g., Ferree et al. 2019). Haploidiploid organisms may thus have a potential route for an evolutionary transition to obligate parthenogenesis that is not available to organisms: The pathways for the modified meiosis may be re-used for oogenesis, which might result in unreduced, diploid eggs. Third, the particular species studied here regularly undergoes inbreeding by brother-sister mating within their hosts. Homozygosity, including at the sex determination locus (Engelstädter 2008), is therefore expected to have less negative effects in this species compared to many other, non-inbreeding haplodipoids (see also Little et al. 2017). This particular species may therefore be less affected by loss of heterozygosity, which occurs in a fashion similar to self-fertilization under many forms of non-clonal parthenogenesis.
Indeed, the study also addresses the mechanisms underlying parthenogenesis in the species. Surprisingly, the authors find that parthenogenetically produced females are likely produced by two distinct genetic mechanisms. The first results in clonality (maintenance of the maternal genotype), whereas the second one results in a loss of heterozygosity towards the telomeres, likely due to crossovers occurring between the centromeres and the telomeres. Moreover, bacterial infections appear to affect the propensity of parthenogenesis but are unlikely the primary cause. Together, the finding suggests that parthenogenesis is a variable trait in the species, both in terms of frequency and mechanisms. It is not entirely clear to what degree this variation is heritable, but if it is, then these results constitute evidence for low-frequency existence of variable and heritable parthenogenesis phenotypes, that is, the raw material from which evolutionary transitions to more regular forms of parthenogenesis may occur.
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Capdevielle Dulac C, Benoist R, Paquet S, Calatayud P-A, Obonyo J, Kaiser L, Mougel F (2022) Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process? bioRxiv, 2021.12.13.472356, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.12.13.472356
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Ferree PM, Aldrich JC, Jing XA, Norwood CT, Van Schaick MR, Cheema MS, Ausió J, Gowen BE (2019) Spermatogenesis in haploid males of the jewel wasp Nasonia vitripennis. Scientific Reports, 9, 12194. https://doi.org/10.1038/s41598-019-48332-9
van der Kooi CJ, Matthey-Doret C, Schwander T (2017) Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods. Evolution Letters, 1, 304–316. https://doi.org/10.1002/evl3.30
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Stalker HD (1954) Parthenogenesis in Drosophila. Genetics, 39, 4–34. https://doi.org/10.1093/genetics/39.1.4
Vorburger C (2014) Thelytoky and Sex Determination in the Hymenoptera: Mutual Constraints. Sexual Development, 8, 50–58. https://doi.org/10.1159/000356508
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Christoph Haag (2022) The potential evolutionary importance of low-frequency flexibility in reproductive modes. Peer Community in Evolutionary Biology, 100141. https://doi.org/10.24072/pci.evolbiol.100141
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. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
Evaluation round #2
DOI or URL of the preprint: https://www.biorxiv.org/content/10.1101/2021.12.13.472356v4
Version of the preprint: 4
Author's Reply, 11 May 2022
Decision by Christoph Haag, posted 25 Apr 2022
Dear Dr. Capdevielle Dulac,
I have read revised preprint as well as the response letter, explaining how you accommodated the points raised by the reviewers. I am satisfied that the revision successfully addresses these points (most of which were already minor) and am therefore happy to further consider your preprint for recommendation. That said, from my own reading, I have come across a number of additional points, which I would like you to consider in a further revision. I hope they will help to further improve the preprint.
Best wishes, and many thanks for submitting to PCI Evol Biol,
L. 55: add “than in others” after “in some taxa”
L. 57-59: Perhaps add here (or elsewhere) that, in addition to egg development without fertilization, haplodiploids also have evolved spermatogenesis with aborted first meiotic division (e.g., Ferree et al. 2019. Sci Rep 9, 12194). In diploids, aborted (or suppressed) meiosis I is one of the possible thelytokous mechanisms leading to maintenance of centromeric heterozygosity or to 100% heterozygosity maintenance if recombination is suppressed. Adoption of the pathways for this type of modified meiosis (already present in males) for oogenetic meiosis may contribute to favouring evolution of telytoky in haplodiploids.
Paragraph starting on L. 62 and elsewhere: the description of the different parthenogenetic mechanisms is now much improved. Still, a few further clarifications may be needed. In particular, I suggest using “Clonal apomixis” or “mitotic apomixis” instead of just “apomixis”: The reason is that the strict definition of apomixis also includes certain parthenogenesis modes that may be non-clonal (i.e., can lead to loss of heterozygosity): The term “apomixis” just means that there is no fusion of cells, so suppressed meiosis I and suppressed meiosis II are also apomictic modes of reproduction (“meiotic apomixis” in Archetti 2010). I know that the different terms are not always used in the same way and that there is a lot of confusion. But it’s perhaps better not to add to it. Also, the difference between “endoreplication” and “endomitosis” is unclear. They are probably the same, at least regarding their use here (also sometimes called “endoreduplication”), so it is better to use just a single term throughout. Finally, I agree that it is not needed to explain in detail the degree of heterozygosity loss or retention under the different mechanisms, but it would be good to provide a few references on the topic (sentence L.80-83).
L. 200 and following paragraph: Define “parthenogenetic female” or probably better use “parthenogenetically produced females” (here and elsewhere in the manuscript), it is not much longer, but substantially more explicit.
L. 235 and L. 248: in each case, specify which or the two protocols.
Fig. 1: I suggest “Clonal apomixis” and “E.g., mitosis” instead of “Apomixis” and “mitosis”. Note that also classical automixis with central fusion can result in fully clonal offspring if recombination is fully suppressed. Perhaps add this note to the figure legend.
L. 264: Here the formulation “parthenogenetic daughters” is particularly unclear: Does “females that produced parthenogenetic daughters” have the same meaning as “females that parthenogenetically produced daughters”? if so, the definition that they are the same should be given before.
Table 1: The header of the last column is unclear (something wrong with the formulation “in the offspring presenting females”). Also, for the percentages (columns 3 and 5), should be specified “of …” (all females tested, all offspring) either here or in the table legend.
L. 305: Perhaps add “tested” to the end of the line.
Table 3: “female sex-ratio” is unclear do you mean proportion of females among all offspring?
L 329 (twice): Here, probably “progeny” is meant instead of offspring (“an offspring” is one individual, 10 offspring 10 individuals, but a progeny is all of the offspring of a given individual)
L. 330: unclear if 773 males were only from the three progenies that contained at least one female offspring or the total across the 10 progenies.
L. 339: perhaps better “along with 6653 males” instead of “for 6653 males”
L 339: “63 SNPs” instead of “63 SNP”.
L. 386: “fertilization” instead of “fecundation”
L. 397: N is probably the number of females tested not the number of offspring analyzed(?)
L. 401: “virgin Makindu mothers” instead of “Makindu virgin mothers”
L. 417: “non-zero” instead of “not null”.
L. 428-430: Sentence unclear. What is meant by “in a common acceptation”? and isn’t that the definition for obligate parthenogenesis?
L. 442: low frequency thelytoky “appears to be” (instead of “may be”) and “rather than” instead of “but not”. You may also add that they had similar fertility as the sexually produced daughters.
L. 445: “with an” adaptive benefit (instead of “due to its”)
L. 446: “confronted with” (instead of “confronted to”)
L. 448: “a honey bee” (instead of “an honey bee”)
L. 448-449: “egg-laying worker” (instead of “laying worker”)
Paragraph starting on line 489: I am not convinced that the results “strongly suggest” that two different mechanisms are at work. The low probability of single process was obtained under the assumption of Poisson-distributed numbers of crossovers. An alternative might be variable (overdispersed) crossover numbers (or locations) among different meioses: central fusion and suppression of meiosis I both result in fully clonal offspring (i.e., 100% heterozygosity retention, if no recombination occurs or if crossover locations are terminal to the last markers). Sure, all these meiosis occurred in F1 of crosses between two divergent inbred lines, so one doesn’t expect too much segregating variation. However, some segregating variation may persist, and crossover numbers (or locations) may also be plastic (as indicated by a single female that produced both daughters both clonally and non-clonally. The possibility that two different mechanisms are at work is interesting to discuss, but in my opinion, it is not needed to invoke any complicated mechanism such as inverted meiosis.
L. 512: What is the evidence that recombination rate was the same as under sexual reproduction?
L. 528: Reformulate the first sentence
L. 553: Meaning of “functional apomixis” unclear.
L. 572: “parthenogenesis” (instead of “situations”).
Evaluation round #1
DOI or URL of the preprint: https://www.biorxiv.org/content/10.1101/2021.12.13.472356v3
Version of the preprint: 3
Author's Reply, 08 Apr 2022
Decision by Christoph Haag, posted 18 Feb 2022
Dear Dr Capdevielle Dulac,
Thank you for submitting your preprint "Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?" to PCI Evol Biol. Your work has now been considered by two reviewers, whose comments are enclosed. As you will see, the reviews are largely positive, and, based on these reviews as well as my own reading, I am happy to further consider your preprint for recommendation. However, before reaching a final decision, I would like you to revise your manuscript according to the recommendations by the reviewers. Furthermore, from my own reading, I would also like you to consider the following points in your revision.
1. The general evolutionary implications of the findings, beyond those specific to the study system, should be explained in more detail, in my opinion. Indeed, both the description of the aims of the study (end of introduction) and the conclusions are highly system-specific, and a clear explanation of the broader implications are missing also elsewhere. To be honest, I would find it somewhat difficult to write a recommendation for a general evolutionary readership based on the current preprint. Nonetheless, there clearly is a potential to present a broader perspective on the results, and some elements are indeed present in various parts of the manuscript. In other words, it would be good to assemble these elements into some more explicit statements of the general evolutionary implications of the study.
2. The figure explaining the different possible modes of parthenogenesis, as well as the corresponding text would need careful revision: (i) Several mechanisms of parthenogenesis are missing, (ii) apomixis is not necessarily equal to mitosis and is not the only way by which clonality can arise, and (iii) the genetic consequences of the different modes of parthenogenesis strongly depend on the amount of recombination. The whole topic is somewhat problematic as many different terms exist and because they are not always employed in the same way. In particular, from a cytological point of view, automixis is defined as normal meiosis followed by fusion of meiotic products (see for instance Archetti J. Hered. 2010). From a genetic point of view, suppression or abortion of one of the meiotic divisions is equivalent to central fusion automixis (suppression/abortion of meiosis I) or terminal fusion automixis (suppression/abortion of meiosis II). However, as there is no fusion in these cases, they are often regarded as apomixis (“meiotic apomixis” in Archetti 2010), especially by cytologists (the term "apomixis" means that there is no fusion). Furthermore, both suppression/abortion of meiosis I and central fusion automixis result in clonal offspring when there is no recombination as does also pre-meiotic doubling (or “endomitosis”) if pairing occurs exclusively between sister chromosomes. These issues should be better reflected in the figure and in the interpretation of the results. Note also that inversed meiosis with terminal fusion is genetically exactly the same as normal meiosis with central fusion (see for instance Archetti 2022 J Evol Biol. 35:40–50). So perhaps it is not needed to complicate matters even more.
3. Parts of the text, most notably in the discussion, could be streamlined. In particular, the discussion of issues not directly related to the results should be kept minimal. Also, please check the entire text carefully for minor language imprecisions.
4. “Presence of parthenogenetic females among the daughters of mated females”: In this section I did not understand why only mixed broods were considered. What was the reason for excluding female-only broods?