New Results

Extremely widespread parthenogenesis and a trade-off between alternative forms of reproduction in mayflies (Ephemeroptera)

Maud Liegeois, Michel Sartori, Tanja Schwander
doi: https://doi.org/10.1101/841122

Abstract

Studying alternative forms of reproduction in natural populations is of fundamental importance for understanding the costs and benefits of sex. Mayflies are one of the few animal groups where sexual reproduction co-occurs with different types of parthenogenesis, providing ideal conditions for identifying benefits of sex in natural populations. Here, we establish a catalogue of all known mayfly species capable of reproducing by parthenogenesis, as well as mayfly species unable to do so. Overall, 1.8% of the described species reproduce parthenogenetically, which is an order of magnitude higher than reported in other animal groups. This frequency even reaches 47.8% if estimates are based on the number of studied rather than described mayfly species. In terms of egg-hatching success, sex is a more successful strategy than parthenogenesis, and we found a trade-off between the efficiency of sexual and parthenogenetic reproduction across species. This means that improving the capacity for parthenogenesis may come at the cost of being less able to reproduce sexually, even in facultative parthenogens. Such a trade-off can help explain why facultative parthenogenesis is extremely rare among animals despite its potential to combine the benefits of sexual and parthenogenetic reproduction. We argue that parthenogenesis is frequently selected in mayflies in spite of this probable trade-off because their typically low dispersal ability and short and fragile adult life may frequently generate situations of mate limitation in females. Mayflies are currently clearly underappreciated for understanding the benefits of sex under natural conditions.

INTRODUCTION

The evolution and maintenance of sexual reproduction has been one of the major questions in evolutionary ecology for the last decades (e.g., Agrawal, 2006; Otto, 2009; Jalvingh et al., 2016). Sex is associated with profound costs (reviewed in Lehtonen et al., 2012), yet it is the most widespread reproductive mode among animals. Female-producing parthenogenesis (thelytoky) would largely avoid the costs associated with sex, yet only a minority of animals are known to reproduce parthenogenetically. Whether this minority is small or rather just slim remains however unknown as there are only two quantitative estimates (based on species lists) of the frequency of parthenogenesis (i.e., in vertebrates: White, 1973; Vrijenhoek, 1998; and in haplodiploids: van der Kooi et al., 2017). This is unfortunate as such species lists are invaluable for addressing when and how parthenogenetic reproduction is favoured over sex in natural populations (e.g., Ross et al., 2013; van der Kooi et al., 2017) and thus for helping to solve the paradox of sex. In this review, we provide such a quantitative estimate by summarising the current knowledge on sexual and parthenogenetic reproduction in Ephemeroptera (mayflies), as a first step towards developing this group for the study of benefits of sex in natural populations.

Mayflies constitute one of the most basal (early diverging) lineage of insects (Edmunds and McCafferty, 1988), their origin dating back to ~300 Mya (Brittain and Sartori, 2009). Widespread around the world with 3’666 described species (42 families, 472 genera; adapted from Sartori and Brittain, 2015; MS pers. com.), they are well studied for being an important link in the food chain, for their use for fly fishing (Knopp and Cormier, 1997), and for their potential as bioindicators of water quality (Bauernfeind and Moog, 2000). Mayflies do not feed as adults, relying solely on the reserves accumulated during their aquatic larval stages. Adult life span is extremely short, lasting from few hours to some days depending on the species. Because of their typically low dispersal ability and their short and fragile adult life, mayflies have restricted opportunities for reproduction, which we argue is one of the factors that may have selected for the evolution of parthenogenesis in this group. Parthenogenesis in mayflies can be largely accidental (i.e., tychoparthenogenesis), facultative or ‘obligate’ (see Box 1). Furthermore, a single species can feature mixed reproduction (some females reproduce sexually, others parthenogenetially), either sympatrically or in allopatry (i.e., geographical parthenogenesis).

We conducted a detailed literature review to establish a catalogue of all (to the best of our knowledge) mayfly species capable of reproducing parthenogenetically, and study whether the frequency of parthenogenesis varies among mayfly clades. We then use this catalogue to conduct cross-species comparisons with respect to the cellular mechanisms of parthenogenesis, how the capacity for parthenogenesis affects population sex ratios, as well as the geographical distribution of sexual and parthenogenetic populations.

Box 1.
Box 1. Three forms of female-producing (thelytokous) parthenogenesis in mayflies.

A) Tychoparthenogenesis or “spontaneous parthenogenesis”, occurs in sexual species (typically less than 10% of unfertilised eggs develop through parthenogenesis). Given the low hatching success of unfertilised eggs, population sex ratios remain equal. B) Facultative parthenogenesis, when an egg may either be fertilised or develop parthenogenetically. The hatching success of unfertilised eggs in this case is intermediate (typically 10-75%), leading to female-biased population sex ratios. C) Under ‘obligate’ parthenogenesis, eggs always develop parthenogenetically and likely cannot be fertilised, with a hatching success typically higher than 75%. Only females are present in these populations. Note that an individual species can feature multiple forms of parthenogenesis, in the same or different populations.

MATERIAL AND METHODS

Data collection

The species list was compiled by collecting information from the literature on different websites: Google Scholar1, Web of Science2, Ephemeroptera Galactica3 and Ephemeroptera of the world4. Starting with four previous reviews (Degrange, 1960; Humpesch, 1980; Sweeney and Vannote, 1987; Funk et al., 2010) that allowed us to compile a first list of 78 mayflies species studied for their reproductive mode, our survey combined with personal communications and observations generated a list of 136 species, as described in our database (Table 1, Appendix). When available for a given species, information on its geographical distribution, cytological mechanism of parthenogenesis and sex determination was included in the database (Appendix).

View this table:
Table 1. Frequency of parthenogenesis and sex determination in Ephemeroptera taxa.

Only families with at least one species studied for its parthenogenetic capacity are shown Seventeen families out of 42 (40.5%) have been studied. The the total numbers of described species have been adapted from Sartori and Brittain (2015) and updated (MS personal communication).

Classification of parthenogenesis

To classify mayfly species by forms of parthenogenesis (Box 1), we focused on the hatching rate of unfertilised eggs. We defined two main categories according to this rate: “sexual species” (including species with tychoparthenogenesis), when less than 10% of unfertilised eggs hatch (typically 0-5.3% for population means), and “parthenogenetic species”, when hatching success of unfertilised eggs is higher than 10% (typically 18.5-97.3% for population means). Parthenogenetic species include all species with facultative parthenogenesis, ‘obligate’ parthenogenesis and mixed reproduction. Note that species with mixed reproduction have low population-average hatching success of unfertilised eggs when sexual and parthenogenetic females occur in sympatry (see results). We also considered species as parthenogenetic if female-only populations were reported in the literature, even if these species were not directly tested for their parthenogenetic capacity (this was the case for 18 of the 136 species in the database).

Within parthenogenetic species, we further distinguished ‘obligate’ from facultative parthenogens. Excluding rare events of sex in putatively obligate pathenogens is difficult (reviewed in Schurko et al., 2009). We used the term obligate parthenogens for species where no males are known, or where rare males (typically <0.1% of all individuals) are most likely vestiges of sexual reproduction (van der Kooi and Schwander, 2014), indicating that parthenogenesis is the main form of reproduction. We also found very rare mentioning of deuterotoky (where both males and females are produced parthenogenetically). Specifically, the baetid species Centroptilum luteolum, Acerpenna pygmaea, Acerpenna macdunnoughi and Anafroptilum semirufum were inferred to be deuterotokous in breeding studies (Degrange, 1956; Funk et al., 2010) because parthenogenetic broods contained high frequencies (2-17%) of males. Occasional deuterotoky is also the most likely explanation for the occurrence of rare males in ‘obligately’ parthenogenetic species as mentioned above. It is currently unclear how such males are produced (e.g., via environmental influences on sex determination or X-chromosome losses in species with XX/X0 sex determination). The few known deuterotokous species are counted as parthenogenetic species in our classification.

Statistical analyses

We first verified that our classification into sexual (with or without tychoparthenogenesis) and parthenogenetic species (facultative, mixed and obligate) was biologically meaningful, by comparing the distribution of hatching successes of unfertilised eggs for different groups (Fig. 1A). We then tested whether species with high egg-hatching successes were often characterised by female-biased population sex ratios, by using a quasibinomial Generalised Linear Mixed Model (GLMM) with the R v.3.3.3 (R Development Core Team, 2017) ‘MASS’ (Venables and Ripley, 2002) and ‘car’ (Fox and Weisberg, 2011) packages. We then compared the prevalence of parthenogenetic species among mayfly families, using the most recent phylogeny available (Ogden et al., 2019). Lack of phylogenetic information at lower taxonomic levels precluded further analyses. In order to obtain the most representative frequency estimate for the group, we also used the inventory of sexual species in our analyses. Indeed, the two available previous estimates of the frequency of parthenogenesis among animals (White, 1973; Vrijenhoek, 1998; van der Kooi et al., 2017) assumed that all described species without evidence for parthenogenesis were sexual. However, this assumption severely underestimates the frequency of parthenogenesis. To account for this underestimation, we generated two frequency estimates, one using the total number of described mayfly species, and one using only species where the reproductive mode was studied. We thus tested whether variations in the frequency of parthenogenesis among families were explained by their phylogenetic relatedness by using binomial Generalised Linear Models (GLMs) and Tukey tests with the ‘multcomp’ (Hothorn et al., 2008) package. In addition, we tested whether the frequency of parthenogenesis in mayflies varies among the six broad geographical regions: Nearctic, Palearctic, Neotropical, Afrotropical, Oriental and Australasian (see map in Table 2). Finally, we tested for potential trade-offs between parthenogenetic and sexual reproduction by studying hatching rate of fertilised and unfertilised eggs at the population level of a given species (Figure 5).

View this table:
Table 2.

World distribution of parthenogenesis in Ephemeroptera.

Figure 1.
Figure 1. A) Population-average hatching successes of unfertilised eggs according to the species’ reproductive modes.

sex: Sexual Reproduction, fac: Facultative parthenogenesis, obl: ‘Obligate’ parthenogenesis, mixed: Mixed reproduction (in sympatry and/or in allopatry). n: number of females tested for a given population. B) Population-level correlation between unfertilised egg-hatching successes and sex ratios (Cor=0.72, p-value <0.001).

RESULTS

Unfertilised egg-hatching successes and population sex ratios

Analysing the information we collected in our database revealed that the parthenogenetic capacity of females varied widely between and within populations (see Appendix for details). Nevertheless, our classification into sexual (with or without tychoparthenogenesis) and parthenogenetic species (facultative or obligate) is biologically meaningful, given the largely non-overlapping values for population-average hatching successes of unfertilised eggs (Figure 1). Note that some species with mixed reproduction show a low population-average hatching success of unfertilised eggs when sexual and parthenogenetic females occur in sympatry (e.g., average of 5.7% for one population of Stenonema femoratum, with egg-hatching successes varying among females from 0 to 77.9%). In order to determine whether a higher capacity for parthenogenesis translates into female-biased population sex ratios, we used species where both sex ratios and unfertilised egg-hatching successes were studied in the same populations. In these species, the parthenogenetic capacity and population sex ratios were significantly positively correlated (Fig. 1B, cor=0.72, p-value <0.001). The parthenogenetic capacity of females in strongly biased populations (>60% of females) was always very high (median: 83.4%, range: 40.4-97.3%), except for the species with mixed reproduction in sympatry as mentioned above (median: 7.8%, range: 3.3-15.5%). Conversely, unbiased population sex ratios were not indicative of species with obligate sexual reproduction, as they frequently comprised females with a high parthenogenetic capacity (Figure 1).

Frequency of parthenogenesis among mayflies

Parthenogenesis occurs in all well-studied mayfly families (Table 1, Fig. 3). We were able to classify the reproductive mode of 136 species from 17 families (Table 1, see Appendix for details). Seventy-one of these species are sexual (from 16 families), and 38 of these are able to perform tychoparthenogenesis, while 65 species are parthenogenetic (from 11 families). Assuming the 3’666 described mayfly species without information concerning their reproductive mode are sexual, 1.8% of all mayfly species are able to reproduce parthenogenetically, which is at least an order of magnitude higher than the available estimate for vertebrates (0.1%, White, 1973; Vrijenhoek, 1998), and comparable to the frequencies in other arthropod orders. For example, the frequency of parthenogenesis in orders with haplodiploid sex determination varies from 0 to 1.5% (van der Kooi et al., 2017). However, if one uses the frequency estimates based on the number of mayfly species studied for their reproductive mode (n=136), the estimated frequency of parthenogenesis reaches 47.8% (Fig. 2), being about 25 times higher. These findings suggest that half of the mayfly species might be able to reproduce parthenogenetically, or even, that most mayflies are able to reproduce at least by tychoparthenogenesis (75.7% of the studied species).

Figure 2.
Figure 2. Frequency of parthenogenesis among described mayfly species (A) and among species studied for their reproductive mode (B).

Less than four percent of the mayfly species have been studied for their reproductive mode. Parthenogenesis (warm colours): facultative (orange), ‘obligate’ (red) and mixed reproduction (purple). Sexual reproduction (cold colours): ‘obligate’ sexual reproduction (green) and sexual reproduction with tychoparthenogenesis (blue). At least 47.8% of the studied species are able to reproduce parthenogenetically.

Figure 3.
Figure 3. Phylogenetic distribution of parthenogenesis among mayfly families.

Parthenogenetic species (facultative, obligate and mixed), Sexual species (with or whithout tychoparthenogenesis), Families without information regarding species’ reproduction. The families Heptageniidae, Leptophlebiidae and Ephemeridae show a low propensity for parthenogenesis, whereas the families Baetidae, Ameletidae and Ephemerellidae show a high propensity for parthenogenesis (see main text for details). Phylogeny adapted from Ogden et al. (2009, 2019).

Parthenogenesis occurs in an array of families and genera without any evidence for phylogenetic clustering (Fig. 3). A similar pattern is observed in haplodiploid taxa (van der Kooi et al., 2017). These findings suggest that putative predispositions for the evolution of parthenogenesis do not have a deep phylogenetic inertia within the studied groups. However, clustering occurs at lower taxonomic levels as the proportion of parthenogenetic species varies significantly among mayfly families (p-value <0.001). Indeed, parthenogenetic mayfly species are rarer in the families Heptageniidae, Leptophlebiidae and Ephemeridae (<1.5% among the described mayfly species, or <30% among the one studied for their reproductive mode), than in the families Baetidae, Ameletidae and Ephemerellidae (>3.0% or >60%).

Geographical parthenogenesis

The term geographical parthenogenesis is used when parthenogenetic populations are found at higher altitudes or latitudes than their sexual counterparts, in harsher environmental conditions or have wider distributions and/or ecological niches (Vandel, 1928). Such different distributions of sexual and asexual species could provide insights into ecological conditions that favour sex or parthenogenesis in natural populations, but quantitative comparisons are scarce (reviewed in Tilquin and Kokko, 2016).

Considering very broad geographical scales and among-species comparisons, we found no evidence for geographic clustering of parthenogenetic species. The six regions compared comprised approximately equal proportions of studied parthenogenetic species (Table 2, see Appendix for details). However, even if such differences existed, we would not be able to uncover them with the currently available data. Indeed, among the 136 studied species, 117 come from Nearctic and Palearctic regions (86%), with very little data available for the remaining regions of the world.

Considering within-species comparisons at smaller geographical scales, there are at least 18 mayfly species (27.7% of the parthenogenetic species) with both sexual and parthenogenetic populations (see Appendix for details). Two of them feature geographical parthenogenesis, but with distinct distribution differences between parthenogens and sexuals. Parthenogenetic populations of Eurylophella funeralis (Ephemerellidae) mostly occur at the periphery of the species ranges in North America (Sweeney and Vannote, 1987), while parthenogenetic populations of Ephemerella notata (Ephemerellidae) occur at lower latitudes than sexual ones in Poland (Glazaczow, 2001). One of the 18 species does not feature geographical parthenogenesis. Indeed, no geographical pattern is observed for Ephoron shigae (Polymitarcyidae), a species where sexual and parthenogenetic populations broadly overlap in Japan (Watanabe and Ishiwata, 1997). Finally, for 15 of the 18 species where sexual and parthenogenetic populations are known to occur in separate geographical areas, the number of described populations is too small to distinguish between a systematic distribution difference from a patchy distribution of sexual and parthenogenetic populations (Appendix).

More than two cases of geographical parthenogenesis likely exist in mayflies but are not detected because of a lack of studies, especially in the southern hemisphere. However, it seems that geographical parthenogenesis is not necessarily associated with particular ecological factors, as is the case in most other taxonomic groups studied thus far (Tilquin and Kokko, 2016).

Cytological mechanisms of parthenogenesis in mayflies

In animals, different cytological mechanisms can underlie thelytokous parthenogenesis, which vary with respect to their consequences on heterozygosity in offspring (reviewed in Suomalainen et al., 1987). In mayflies, some of these mechanisms have been identified or suggested, but studies remain scarce. Nevertheless, the available information suggests that obligate parthenogens use cytological mechanisms that potentially allow for maintenance of heterozygosity across generation (but see Jaron et al., 2018), while facultative parthenogens are invariably automictic and produce parthenogenetic offspring that are highly homozygous relative to sexual offspring. Specifically, nine out of the 10 studied ‘obligately’ parthenogenetic mayflies are functionally clonal without a detected loss of heterozygosity between generations (Sweeney and Vannote, 1987; Sweeney et al., 1993; Funk et al., 2006, 2008, 2010). Three mechanisms can be responsible of the complete maintenance of heterozygosity between generations: apomixis (no meiosis occurs – mitotic parthenogenesis), endoduplication, or automixis with central fusion (without recombination). Which one(s) of these mechanisms occur in mayflies is currently unknown. The cytological mechanism of the remaining species, E. shigae in Japan, was suggested to be automixis with terminal fusion (Sekiné and Tojo, 2010b), indicating that some ‘obligate’ parthenogens might not be clonal.

All seven studied facultatively parthenogenetic mayflies are automictic (Appendix). Indeed, for the populations with both males and females of seven Baetidae species (Acerpenna macdunnoughi, A. pygmaea, Anafroptlilum semirufum, Labiobaetis frondalis, Neocloeon alamance, Procloeon fragile, P. rivulare) parthenogenesis appears to be automictic with terminal or central fusion (with recombination), given the partial loss of heterozygosity between generations, but further details are not known (Funk et al., 2010). Finally, the cytological mechanism in Ephoron eophilum (Polymitarcyidae), a mostly sexual species with some facultatively parthenogenetic females (i.e., mixed reproduction in sympatry) is either automixis with terminal fusion (without recombination) or gamete duplication, where complete homozygosity is achieved in one generation (Sekiné et al., 2015). Cytological mechanisms of parthenogenesis in mayflies clearly require additional studies, but the major mechanisms identified to date are summarised in Figure 4.

Figure 4.
Figure 4.

Cytological mechanisms identified to date in mayflies and possible transition between parthenogenesis forms.

Overall, mayfly species are better at reproducing sexually than asexually (measured as egg-hatching success, Fig. 5A, p-value <0.001). Only in obligate parthenogens is egg-hatching success decreased upon mating, presumably because (even partial) fertilisation interferes with normal development of asexual eggs. Furthermore, there is a significant negative correlation between hatching rate of fertilised and unfertilised eggs at the population level of a given species (Fig. 5B, cor=-0.50, p-value=0.02). This negative correlation suggests that there are trade-offs between parthenogenetic and sexual reproduction, meaning that improving the capacity for parthenogenesis may come at the cost of being less able to reproduce sexually, even in facultative parthenogens. If such a trade-off indeed exists, it could help explain why facultative parthenogenesis is extremely rare among animals in spite of its potential to combine the benefits of sexual and parthenogetetic reproduction.

Figure 5.
Figure 5. A) Hatching success of fertilised and unfertilised eggs for species with different reproductive modes and mating status.

n: number of females tested for a given population; B) Trade-off between parthenogenesis and sexual reproduction of a given population (cor=-0.50, p-value=0.02).

Origins of ‘obligate’ parthenogenesis in mayflies

There are at least four ways in which parthenogenetic lineages could arise from sexual species in animals: (1) Hybridisation between two sexual species, which is the major route to parthenogenesis in vertebrates (Avise et al., 1992); (2) Contagious origin from pre-existing parthenogenetic lineages, where males produced by parthenogenetic species generate new lineages by mating with sexual females (e.g., in aphids Jaquiéry et al., 2014; and water fleas Xu et al., 2015); (3) Infection by microorganisms (e.g., Wolbachia, Cardinium, Rickettsia), mostly in species with haplodiploid sex determination (reviewed in Ma and Schwander, 2017) and (4) Spontaneous transitions through mutations, for example with tychoparthenogenesis as a first step (Carson et al., 1957; Kramer and Templeton, 2001; Schwander and Crespi, 2009; Schwander et al., 2010).

In mayflies, there is no evidence of parthenogenesis induced by hybridisation or endosymbiont infection, but there is very little data informing on the origins of parthenogenesis. An hybrid origin seems unlikely because it usually results in high levels of heterozygosity (recently reviewed in Jaron et al., 2018) which is not the case for unisexual populations of the mayfly species studied so far (Sweeney and Vannote, 1987; Funk et al., 2006; Sekiné and Tojo, 2010b). Endosymbiont induced parthenogenesis is also unlikely in mayflies because parthenogenesis in this group is often facultative, while endosymbiont infection normally causes obligate parthenogenesis (reviewed in Ma and Schwander, 2017). In addition, sex determination is male heterogamety (not haplodiploïdy, Table 1, see Appendix for details), further reducing the probability for endosymbiont-induced parthenogenesis.

In mayflies, it has been speculated that facultative and obligate parthenogenesis originates from tychoparthenogenesis (Sweeney and Vannote, 1987; Tojo et al., 2006). Although this is a plausible hypothesis given how widespread tychoparthenogenesis is among mayflies (27.9% of the studied species, Fig. 2, see Appendix for details), there is no actual evidence for this suggestion. Indeed, there is currently very little information available that allows inferring how (facultative or obligate) parthenogenesis evolved in any of the known mayfly species. Nevertheless, because of their low dispersal ability and their short and fragile adult life, mayflies have restricted opportunities for reproduction, which may frequently generate situations of mate limitation in females. Mate limitation has been shown to favour parthenogenesis in other insect species (Schwander et al., 2010), and is very likely to also select for parthenogenesis in mayflies, in spite of the probable trade-off with sexual reproduction we highlighted above.

Fate of sexual traits in ‘obligate’ parthenogenetic mayflies

Sexual traits in asexual species decay more or less rapidly depending on whether they become costly or neutral upon transitions to parthenogenesis (reviewed in van der Kooi and Schwander, 2014). Selection favours the reduction of costly traits, contrary to neutral traits which decay via drift. For example, sexual traits which could decay in parthenogenetic females mayflies are: (1) pheromones, (2) the capacity to produce males, (3) the ability to fertilise their eggs, and (4) the synchrony of emergences.

Sex pheromones are chemical signals involved in mate choice (reviewed in Johansson and Jones, 2007) that can disappear in asexual lineages (e.g., Schwander et al., 2013; Tabata Jun et al., 2017). However, there are apparently no volatile pheromones in mayflies, with mate choice and species recognition based on visual signals and tactile recognition (Landolt et al., 1997; MS pers. com.).

Occasional production of males has been reported in a range of ‘obligately’ parthenogenetic mayfly species (e.g., in Ameletus ludens Clemens, 1922; Needham, 1924; and in Neocloeon triangulifer Funk et al., 2006, 2010) similar to most parthenogenetic species in other animal groups (van der Kooi and Schwander, 2014). In species with male heterogamety, male development in parthenogenetic lineages likely follows the accidental loss of an X chromosome during oogenesis (Schwander et al., 2013). Accidental males produced by parthenogenetic females are often still able to fertilise eggs of females from sexual populations (van der Kooi and Schwander, 2014), but there is currently little information on the fertility of accidental males in mayflies. If fertile, as shown for two baetid species (Funk et al., 2010), such males could potentially generates new lineages by matings with sexual females (i.e., contagious parthenogenesis as explained above), which could help explain the high frequency of parthenogenesis in mayflies.

The ability of parthenogenetic females to fertilise their eggs is unknown in mayflies overall, as only one species, the baetid Neocloeon triangulifer, has been studied thus far (Funk et al., 2006). In this species, the ability to fertilise eggs is maintained at least at low levels. Viable progeny could be obtained by crossing Neocloeon alamance males (a sexual species with XY male heterogamety) with parthenogenetic N. triangulifer females. In such crosses, 66.6% of offspring were normal, clonal N. tringulifer females with high fertility, suggesting they were produced parthenogenetically from unfertilised eggs. However, the remaining 33.3% were genetically intermediate between the two species (as indicated by allozyme genotypes), suggesting they were hybrids produced from fertilised eggs. Approximately half of this hybrid progeny were females, perhaps triploid, with low fertility, the second half consisted of sterile gynandromorphs (with both male and females morphological characteristics). These findings suggest that even ‘obligately’ parthenogenetic mayfly species still produce haploid eggs, which could explain why there is always a small proportion of unfertilised eggs that never hatch (typically 3-22%), although more data are clearly needed.

Depending on how synchronous the emergences of both sexes are, the temporal windows to find a mate can be affected. Accordingly, obligate parthenogenesis might lead to a decay of the flight activity patterns in mayfly species. Tropical species of Trichoptera and Ephemeroptera appear to follow this theory (Tjønneland, 1970). However, this does not hold for several other mayfly species from temperate regions (e.g., Ameletidae: Ameletus ludens; Baetidae: Neocloeon triangulifer; Ephemerellidae: Ephemerella notata and Eurylophella funeralis), where emergence patterns of parthenogenetic mayflies are at least as synchronous as for sexual species (Sweeney and Vannote, 1982; Glazaczow, 2001). These findings might indicate that synchronisation of emergence is not costly in temperate regions, or that there are other factors such as predation that select for the maintenance of emergence synchrony (Sweeney and Vannote, 1982).

CONCLUSION

We found evidence for parthenogenesis in at least 65 mayfly species, which represent as much as 1.8% of the 3’666 described species. However, this frequency is likely underestimated given that among the 136 species whose reproductive mode was studied, this value reaches 47.8%, currently the highest estimate known in non-cyclical parthenogenetic organisms. Parthenogenesis in mayflies thus appears to be widespread and is certainly an order of magnitude more frequent than in animal groups surveyed thus far. Among the 71 mayflies species found to reproduce sexually, 38 (53.5%) can produce offspring by accidental parthenogenesis (i.e., tychoparthenogenesis). Such accidental parthenogenesis could function as a pre-adaptation for facultative parthenogenesis, which may often be selected in mayflies because their short adult life frequently generates situations of mate limitation.

Additional studies focused on species from areas other than North America and Europe would be necessary to obtain a fully representative overview of the frequency of parthenogenesis in mayflies and for uncovering potential lineage-level or geographical-ecological correlates of parthenogenesis in this group. Additional studies are also needed regarding the cytological mechanisms and the origin of parthenogenesis in mayflies. In spite of these constraints, mayflies are currently clearly underappreciated for their value as outstanding model systems for testing benefits of sex in natural populations.

Acknowledgement

We would like to thank Luca Sciuchetti for his contribution to review the literature and help for building the database. This study was supported by grants PP00P3_139013 and PP00P3_170627 from the Swiss NSF.

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Extremely widespread parthenogenesis and a trade-off between alternative forms of reproduction in mayflies (Ephemeroptera)
Maud Liegeois, Michel Sartori, Tanja Schwander
bioRxiv 841122; doi: https://doi.org/10.1101/841122
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