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Extremely Widespread Parthenogenesis and a Trade-Off Between Alternative Forms of Reproduction in Mayflies (Ephemeroptera)

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Extremely Widespread Parthenogenesis and a Trade-Off Between Alternative Forms of Reproduction in Mayflies (Ephemeroptera) bioRxiv preprint doi: https://doi.org/10.1101/841122; this version posted November 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Extremely widespread parthenogenesis and a trade-off between 2 alternative forms of reproduction in mayflies (Ephemeroptera) 3 4 Maud Liegeois1,2, Michel Sartori2,1 and Tanja Schwander1 5 1Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, 6 Switzerland; emails: [email protected]; [email protected] 7 2Cantonal Museum of Zoology, Palais de Rumine, Place de la Riponne 6, CH-1014 8 Lausanne, Switzerland; email: [email protected] 9 10 11 Abstract 12 Studying alternative forms of reproduction in natural populations is of fundamental 13 importance for understanding the costs and benefits of sex. Mayflies are one of the few 14 animal groups where sexual reproduction co-occurs with different types of parthenogenesis, 15 providing ideal conditions for identifying benefits of sex in natural populations. Here, we 16 establish a catalogue of all known mayfly species capable of reproducing by parthenogenesis, 17 as well as mayfly species unable to do so. Overall, 1.8% of the described species reproduce 18 parthenogenetically, which is an order of magnitude higher than reported in other animal 19 groups. This frequency even reaches 47.8% if estimates are based on the number of studied 20 rather than described mayfly species. In terms of egg-hatching success, sex is a more 21 successful strategy than parthenogenesis, and we found a trade-off between the efficiency of 22 sexual and parthenogenetic reproduction across species. This means that improving the 23 capacity for parthenogenesis may come at the cost of being less able to reproduce sexually, 24 even in facultative parthenogens. Such a trade-off can help explain why facultative 25 parthenogenesis is extremely rare among animals despite its potential to combine the benefits 26 of sexual and parthenogenetic reproduction. We argue that parthenogenesis is frequently 27 selected in mayflies in spite of this probable trade-off because their typically low dispersal 28 ability and short and fragile adult life may frequently generate situations of mate limitation in 29 females. Mayflies are currently clearly underappreciated for understanding the benefits of sex 30 under natural conditions. 31 32 33 Key Words: mayflies, parthenogenesis, natural populations, evolution of sex. 34 bioRxiv preprint doi: https://doi.org/10.1101/841122; this version posted November 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 35 INTRODUCTION 36 The evolution and maintenance of sexual reproduction has been one of the major questions in 37 evolutionary ecology for the last decades (e.g., Agrawal, 2006; Otto, 2009; Jalvingh et al., 38 2016). Sex is associated with profound costs (reviewed in Lehtonen et al., 2012), yet it is the 39 most widespread reproductive mode among animals. Female-producing parthenogenesis 40 (thelytoky) would largely avoid the costs associated with sex, yet only a minority of animals 41 are known to reproduce parthenogenetically. Whether this minority is small or rather just slim 42 remains however unknown as there are only two quantitative estimates (based on species 43 lists) of the frequency of parthenogenesis (i.e., in vertebrates: White, 1973; Vrijenhoek, 1998; 44 and in haplodiploids: van der Kooi et al., 2017). This is unfortunate as such species lists are 45 invaluable for addressing when and how parthenogenetic reproduction is favoured over sex in 46 natural populations (e.g., Ross et al., 2013; van der Kooi et al., 2017) and thus for helping to 47 solve the paradox of sex. In this review, we provide such a quantitative estimate by 48 summarising the current knowledge on sexual and parthenogenetic reproduction in 49 Ephemeroptera (mayflies), as a first step towards developing this group for the study of 50 benefits of sex in natural populations. 51 Mayflies constitute one of the most basal (early diverging) lineage of insects 52 (Edmunds and McCafferty, 1988), their origin dating back to ~300 Mya (Brittain and Sartori, 53 2009). Widespread around the world with 3’666 described species (42 families, 472 genera; 54 adapted from Sartori and Brittain, 2015; MS pers. com.), they are well studied for being an 55 important link in the food chain, for their use for fly fishing (Knopp and Cormier, 1997), and 56 for their potential as bioindicators of water quality (Bauernfeind and Moog, 2000). Mayflies 57 do not feed as adults, relying solely on the reserves accumulated during their aquatic larval 58 stages. Adult life span is extremely short, lasting from few hours to some days depending on 59 the species. Because of their typically low dispersal ability and their short and fragile adult 60 life, mayflies have restricted opportunities for reproduction, which we argue is one of the 61 factors that may have selected for the evolution of parthenogenesis in this group. 62 Parthenogenesis in mayflies can be largely accidental (i.e., tychoparthenogenesis), facultative 63 or ‘obligate’ (see Box 1). Furthermore, a single species can feature mixed reproduction (some 64 females reproduce sexually, others parthenogenetially), either sympatrically or in allopatry 65 (i.e., geographical parthenogenesis). 66 We conducted a detailed literature review to establish a catalogue of all (to the best of 67 our knowledge) mayfly species capable of reproducing parthenogenetically, and study 68 whether the frequency of parthenogenesis varies among mayfly clades. We then use this 69 catalogue to conduct cross-species comparisons with respect to the cellular mechanisms of 70 parthenogenesis, how the capacity for parthenogenesis affects population sex ratios, as well as 71 the geographical distribution of sexual and parthenogenetic populations. 2 bioRxiv preprint doi: https://doi.org/10.1101/841122; this version posted November 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 72 73 74 Box 1. Three forms of female-producing (thelytokous) parthenogenesis in mayflies. A) 75 Tychoparthenogenesis or “spontaneous parthenogenesis”, occurs in sexual species (typically less than 10% 76 of unFertilised eggs develop through parthenogenesis). Given the low hatching success oF unfertilised eggs, 77 population sex ratios remain equal. B) Facultative parthenogenesis, when an egg may either be Fertilised or 78 develop parthenogenetically. The hatching success of unfertilised eggs in this case is intermediate (typically 79 10-75%), leading to Female-biased population sex ratios. C) Under ‘obligate’ parthenogenesis, eggs always 80 develop parthenogenetically and likely cannot be fertilised, with a hatching success typically higher than 81 75%. Only Females are present in these populations. Note that an individual species can Feature multiple 82 forms of parthenogenesis, in the same or different populations. 83 84 MATERIAL AND METHODS 85 Data collection 86 The species list was compiled by collecting information from the literature on different 87 websites: Google Scholar1, Web of Science2, Ephemeroptera Galactica3 and Ephemeroptera 88 of the world4. Starting with four previous reviews (Degrange, 1960; Humpesch, 1980; 89 Sweeney and Vannote, 1987; Funk et al., 2010) that allowed us to compile a first list of 78 90 mayflies species studied for their reproductive mode, our survey combined with personal 1 https://scholar.google.com 2 https://apps.webofknowledge.com 3 www.ephemeroptera-galactica.com 4 www.insecta.bio.spbu.ru/z/Eph-spp/Contents.htm 3 bioRxiv preprint doi: https://doi.org/10.1101/841122; this version posted November 13, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 91 communications and observations generated a list of 136 species, as described in our database 92 (Table 1, Appendix). When available for a given species, information on its geographical 93 distribution, cytological mechanism of parthenogenesis and sex determination was included 94 in the database (Appendix). 95 96 Classification of parthenogenesis 97 To classify mayfly species by forms of parthenogenesis (Box 1), we focused on the hatching 98 rate of unfertilised eggs. We defined two main categories according to this rate: “sexual 99 species” (including species with tychoparthenogenesis), when less than 10% of unfertilised 100 eggs hatch (typically 0-5.3% for population means), and “parthenogenetic species”, when 101 hatching success of unfertilised eggs is higher than 10% (typically 18.5-97.3% for population 102 means). Parthenogenetic species include all species with facultative parthenogenesis, 103 ‘obligate’ parthenogenesis and mixed reproduction. Note that species with mixed 104 reproduction have low population-average hatching success of unfertilised eggs when sexual 105 and parthenogenetic females occur
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