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Abstract

Female-producing parthenogenesis can be induced by endosymbionts that increase their transmission by manipulating host reproduction. Our literature survey indicates that such endosymbiont-induced parthenogenesis is known or suspected in 124 host species from seven different arthropod taxa, with Wolbachia as the most frequent endosymbiont (in 56-75% of host species). Most host species (81%, 100 out of 124) are characterized by haplo-diploid sex determination, but a strong ascertainment bias likely underestimates the frequency of endosymbiont-induced parthenogenesis in hosts with other sex determination systems. In at least one taxon, hymenopterans, endosymbionts are a significant driver of transitions from sexual to parthenogenetic reproduction, with one-third of lineages being parthenogenetic as a consequence of endosymbiont infection. Endosymbiont-induced parthenogenesis appears to facilitate the maintenance of reproductive polymorphism: at least 50% of species comprise both sexual (uninfected) and parthenogenetic (infected) strains. These strains feature distribution differences similar to the ones documented for lineages with genetically determined parthenogenesis, with endosymbiont-induced parthenogens occurring at higher latitudes than their sexual relatives. Finally, although gamete duplication is often considered as the main mechanism for endosymbiont-induced parthenogenesis, it underlies parthenogenesis in only half of the host species studied thus far. We point out caveats in the methods used to test for endosymbiont-induced parthenogenesis and suggest specific approaches that allow for firm conclusions about the involvement of endosymbionts in the origin of parthenogenesis.

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Ma, W. -J.;  Schwander, T.

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  • Comments to the Author Palatable, formatted version of the review attached.

    I. A valuable paper This review provides a synthesis of current knowledge on symbiont-induced parthenogenesis in animals, and extracts and discusses what patterns seem to appear. Information is synthesized in the form of detailed tables (containing host species, symbiont species, sex-determination system of host, whether sexual populations are known, type of parthenogenesis) that also, crucially, incorporate a measure of the certainty of some of this information (what method was used, strength of evidence). The patterns extracted of the data are carefully handled, taking into account uncertainty and still limited data. The writing is clear and the structure satisfying, I found the paper an approachable yet in-depth review.

    My main comment on each of the three aspects of the paper: 1) An up-to-date database of animals with endosymbiont-induced parthenogenesis is very welcome. 2) The discussion of the various methods used for symbiont and mechanism determination and their caveats is useful, and will surely help readers interpret present data more accurately and carefully, and researchers improve their experimental protocols. 3) The discussion of the patterns identified is interesting, but I believe one aim of this review should be to trigger as much reflection as possible, and hence it could be enriched by discussing a few more perspectives.

    Most comments below are not criticisms to be addressed absolutely, but mere suggestions for improvement, and I trust the authors to know better than I which ones are valuable to follow.

    II. Main comments about the content

    • Reproductive polymorphism in haplo-diploid species is discussed in a dedicated paragraph (l 85), but it is not discussed in diplo-diploid species (though the data is present in Table 2). Why not? This gap should be filled, or justified, especially since the next paragraph is about polymorphism in all parthenogenetic species regardless of their sex-determination system.

    • l 93: “reproductive strategies have only been investigated in one or few populations such that sexual populations may have been missed.” Perhaps it would be an appropriate place to mention that inversely, predominantly sexual species with only a few parthenogenetic populations are likely to be undetected as parthenogens.

    • p4-5 about reproductive polymorphism. I find that a discussion of the transmission mechanisms is missing. How are parthenogenesis-inducing symbionts acquired and transmitted? What can be the outcomes of a male mating with an symbiont-carrying female (info also needed l 112)? I think those clarifications about how it spreads should really take place before discussion of reproductive polymorphism page 5. -- l 108: Paragraph about the evolution of resistance to explain reproductive polymorphism: I found that this paragraph was a bit confusing, I think from the lack of background about transmission, and from a few ambiguities that made me stop and think: --- l 112: “mating partners”: they could “mate” without any offspring to be sexually produced. It should be made clear right away that it results in male reproductive success. --- l 113: I think the sentence makes it a bit ambiguous as to whether facultative parthenogenesis is found in other groups. To make sure it is clear I would suggest: “Among species with endosymbiont-induced parthenogenesis, facultative sex is only known in…” --- l 116: “the resistance mechanism in the host increases the production of males, which is favoured in populations with female-biased sex-ratios.” The phrasing is a bit imprecise, especially since in one case, the resistance mechanism is born by the female, and in the other, by the male. Maybe “The resistance mechanism increases the number of sons of its bearer” would be more rigorous ? At any rate, maybe this part of the sentence can be dropped entirely to make the flow simpler, since the fitness implications of producing sons are explained at the end of the paragraph. --- l 124: add ref to the modelling work to support assertion? (Stouthamer 2001)

    • Geographic parthenogenesis has never been investigated in species with symbiont-induced parthenogenesis; whereas reproductive polymorphism, as shown by the authors is common. If the authors gained any insight from the papers they reviewed about potential geographic patterns, or the absence thereof, it would be an interesting point to discuss.

    • p 7, about ways to confirm that parthenogenesis is indeed induced by a symbiont in diplo-diploids. That might be naïve as I don’t know much about what is possible in this respect, but shouldn’t karyotyping the eggs provide at least some circumstantial evidence of the symbiont’s role? If removing the symbiont results in an unviable, but diploid egg, it would be evidence that parthenogenesis has at least some genetic basis.

    • p 8, paragraph about the identity of the symbionts and their proportions. As it is, I think there is a risk that some readers might get stuck at the beginning and start thinking of possible biases before reading on, while some others might actually remember only the statistics, and not the following grain of salt. Suggestions to make its flow more smoothly for the reader: 1) mention at the beginning that methods for identifying bacteria are discussed in the next section. 2) I think the caveats about the data should also be mentioned early on, be it briefly, before the actual statistics

    • p 13-14, about the prevalence of the various types of parthenogenesis, and what can explain them. Encarsia species are well-represented in the dataset (4 sp), maybe it would be interesting to discuss them a bit more? First, the 3 cases with confirmed central fusion are Encarsia + Cardinium (therefore they are pseudoreplicated data points if one is trying to get a feeling of the relative prevalence of each type of parthenogenesis, or the modus operandi of each symbiont; maybe point this out? especially l 338!); second, the fourth species of Encarsia that uses gamete duplication is triggered by Wolbachia, which could be pointed out as well in the paragraph discussing symbiont effect (l 334)

    • p14: paragraph about the high frequency of gamete-duplication in symbiont-induced parthenogenesis compared to genetic parthenogenesis. The argument presented is that gamete-duplication is probably more deleterious than other types of parthenogenesis, since it renders the individual totally homozygous, but that conversely it is also probably the most convenient mechanism to manipulate for a symbiont. It seems to me that another important point is missing. Since nearly all know cases of symbiont-induced parthenogenesis are in haplodiploids, I think a strong argument could relate to the fact that haplodiploids suffer less from inbreeding depression, since all recessive deleterious alleles are expressed in the haploid males and therefore purged (but see Tien15 for how females can still suffer from inbreeding). It is telling that out of the 3 non haplo-diploid species of Table 3, the 2 showing gamete duplication are Coccids, and might have ancestrally displayed Paternal Genome Elimination (for Parthenolecanium, see Ross10; I’m not so sure about Eucalymnatus), in which case males also expressed a hemigenome, allowing the purge to take place. In that case, gamete duplication and the resulting homozygosity is hardly worse than having a male hemizygous genome. Maybe this is a thread worth following. On a related note: l 372: about how gamete duplication would lead to female sex in haplodiploids, due to their sex determination. With complementary sex determination, gamete duplication that results in a homozygous offspring would lead to a male phenotype, therefore it can be worth noting that gamete duplication is not expected under CSD (Heimpel & de Boer)

    • p 15, paragraph about proximate mechanisms. The paragraph is very speculative, so perhaps it would be nice to make it clearer whether the references are to who originally proposed a possibility, or if it is empirical evidence for this given possibility.

    III. Typos and nitpicking

    l 68: “Endosymbiont-induced parthenogenesis” -> the title of this part is uninformative (it’s nearly the title of the paper). Change to something clearer, for example equivalent to “instances of endosymbiont-induced parthenogenesis”…

    l 52: “reasons for why” -> “reasons why”

    l 59: “to establish a database of all species in which parthenogenesis is caused by endosymbiont infection” -> it wouldn’t hurt to add a “known” somewhere in the sentence to emphasize we probably still know only a fraction

    l 74-76: “an approximate estimate for the frequency” -> I suggest changing to “an estimate of the minimum frequency” or “a lower estimate of the frequency”, and adding an explicit statement about the fact that in many species the mechanism behind parthenogenesis has never been investigated (echoing the “at least” l 83). I think clarity is better as you could also have chosen to compute an estimate of the number of endosymbiont-induced cases, among the cases where cause is known.

    l 322: “[among haplo-diploids] not a single species known that features genetically caused parthenogenesis via gamete duplication” …out of? -> missing information: the number of haplodiploids with genetically caused parthenogenesis

    l 181: typo: ->“fourth”

    l 290: coma: oribatib mites, Taberly

    l 300 typo: -> “principle”

    l 362: double parentheses

    l 415: -> “we declare” (x2)

    Tables: Because I find that typos or outdated synonymies very often find their way in such published taxonomic tables, I would recommand a last careful check by the authors.

    Eg: Synonymy: Lecanium cerasifex is now Parthenolecanium cerasifex (source: EOL)

    Typo: Eucalymnatus (source: EOL)

    Table S1: Twice the column “host species” l 6: Aonidiella aurantii -> Hemiptera

    Table S2: typo: -> “reproductive polymorphism” Drosophila albomicans also uses predominantly gamete duplication; it is only facultatively parthenogenetic though, but some populations seem to have a high incidence of parthenogenesis (Chang14)

    References: @ authors or editorial office : Please carefully review references. Species names are often not in italics (not listed). In addition:

    Capitalization missing: 444 capitalization 506 capitalization 572 Capitalization, hyphenation 763 Parthenogenese (capital P Typos in titles: 458 phytophagous 614 Virulence, multiple infections… 718 substantiation 785 Phylogenetic 795 recombination

    Typos in authors’ name 495 DeWayne is a first name, abbreviation should be Shoemaker D.D. 498 3rd name is Frédéric Fleury, should be abbreviated as Fleury, F. 528 Giovanna is one of her 2 first names, abbreviation should be Riparbelli M.G. (also change ref in table 3) 745 Stouthamer

    Referencing: 521 where was the poster presented? 814 and 828 : duplicated reference

    Papers cited in this review: Chang, Chia-chen, et al. "The Persistence of Facultative Parthenogenesis in Drosophila albomicans." PloS one 9.11 (2014): e113275. Ross, Laura, Ido Pen, and David M. Shuker. "Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems." Biological Reviews 85.4 (2010): 807-828. Tien, N. S. H., M. W. Sabelis, and M. Egas. "Inbreeding depression and purging in a haplodiploid: gender-related effects." Heredity 114.3 (2015): 327-332.

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