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 catalog of all known mayfly species capable of reproducing by parthenogenesis, as well as 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, as reproductive modes have thus far been studied in only 17 out of 42 families. We find that sex is a more successful strategy than parthenogenesis (associated with a higher hatching success of eggs), with a trade-off between the hatching success of parthenogenetic and sexual eggs. This means that improving the capacity for parthenogenesis may come at a cost for sexual reproduction. 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.
Different reproductive modes are characterized by costs and benefits which often depend on ecological contexts. Benefits of sex are expected to increase under complex biotic interactions, whereas parthenogenesis can be beneficial for reproductive assurance when females are mate limited. Here, we study how different ecological contexts influence the frequency of sex or parthenogenesis in the facultatively parthenogenetic mayfly Alainites muticus. We first verified that high parthenogenetic frequencies translate into female-biased population sex ratios. We then measured the population sex ratio (a proxy for parthenogenetic capacities), density of individuals (mate limitation) and community diversity (biotic interaction complexity) for 159 A. muticus populations, and used structural equation modeling to investigate their direct and indirect influences on sex ratios. We found no effect of community diversity or altitude on sex ratios. Furthermore, even when females can reproduce parthenogenetically, they generally reproduce sexually, indicating that the benefits of sex exceed its costs in most situations. Sex ratios become female-biased in low population densities, as expected if mate limitation selects for parthenogenesis. Mate limitation might be widespread in mayflies because of their very short adult lifespan and limited dispersal, which can generate strong selection for reproductive assurance and may provide a steppingstone towards obligate parthenogenesis.
Different reproductive modes are characterized by costs and benefits which often depend on ecological contexts. Benefits of sex are expected to increase under complex biotic interactions, whereas parthenogenesis can be beneficial for reproductive assurance when females are mate limited. Here, we study how different ecological contexts influence the frequency of sex or parthenogenesis in the facultatively parthenogenetic mayfly Alainites muticus. We first verified that high parthenogenetic frequencies translate into female-biased population sex ratios. We then measured the population sex ratio (a proxy for parthenogenetic capacities), density of individuals (mate limitation) and community diversity (biotic interaction complexity) for 159 A. muticus populations, and used structural equation modeling to investigate their direct and indirect influences on sex ratios. We found no effect of community diversity or altitude on sex ratios. Furthermore, even when females can reproduce parthenogenetically, they generally reproduce sexually, indicating that the benefits of sex exceed its costs in most situations. Sex ratios become female-biased in low population densities, as expected if mate limitation selects for parthenogenesis. Mate limitation might be widespread in mayflies because of their very short adult lifespan and limited dispersal, which can generate strong selection for reproductive assurance and may provide a steppingstone towards obligate parthenogenesis.
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