Self-fertilization, but not mating strategy, predicts the evolution of sex allocation plasticity in a hermaphroditic flatworm genus

Abstract

Local sperm competition (LSC), which occurs when related sperm compete for access to a given set of eggs, can influence sex allocation (SA) in simultaneous hermaphrodites. Different factors that have been predicted to affect LSC—and hence, optimal SA—include the mating strategy (such as reciprocal mating vs. hypodermic insemination) and the ability to self-fertilize. Moreover, the level of LSC experienced could vary temporally and/or spatially, favouring the evolution of SA plasticity. However, it is unknown how the mating strategy and ability to self-fertilize can influence SA and SA plasticity. Here, we explored this by collecting estimates of SA and SA plasticity for seven species of the flatworm genus, Macrostomum, and performing analyses while controlling for phylogeny. While we found substantial interspecific variation in SA, neither the mating strategy nor the ability to self-fertilize had a significant effect on SA. Next, we estimated standardized effect sizes for SA plasticity in response to i) the presence of mating partners and ii) the strength of LSC for each species, and tested if the mating strategy or ability to self-fertilize predicted these effect sizes. We found considerable interspecific variation in SA plasticity, with some species being highly plastic and others showing no significant plasticity. Moreover, self-fertilization predicted SA plasticity with respect to the presence of mating partners, with SA plasticity being lower for self-fertilizing species. Finally, we showed that interspecific variation in SA is nearly three times higher than intraspecific variation, suggesting that SA estimates in field-collected specimens can, at least to some degree, be interpreted as representing interspecific rather than intraspecific variation. Our study suggests that both SA and SA plasticity can evolve rapidly, with self-fertilization being an important predictor for the latter in Macrostomum.

Evolution and co-evolution of the suck behaviour, a postcopulatory female resistance trait that manipulates received ejaculate

“…These transitions could represent transitional steps towards hypodermic insemination, which might arise as a means to bypass the female control and allow access to the eggs (Charnov, 1979; Brand et al ., 2022b). Moreover, this interpretation is also supported by the finding that there are multiple origins of hypodermic insemination in the genus Macrostomum (Brand et al ., 2022b; Singh & Schärer, 2021). There are at least nine independent shifts from reciprocal mating to hypodermic insemination in Macrostomum , while no transition is observed in the converse direction (Brand et al ., 2022b).…”

“…Species in the genus Macrostomum are small (~0.3 to 3.0 mm body length) aquatic free-living flatworms that are highly transparent, permitting detailed observations of internal structures (for the general morphology see Figure 1A,B). The sperm and eggs are produced in the paired testes and paired ovaries, respectively, with studies documenting inter-and intra-specific variation in both testis and ovary size across the genus (Singh et al, 2020b;Brand et al, 2022a;Singh & Schärer, 2021). The female antrum is located anterior to the male antrum, connected to the outside, respectively, via a female genital opening (also female genital pore or vagina) and the male genital opening (also male genital pore).…”

“…Finally, mating frequency (and possibly mating duration) could be positively correlated with allocation towards the male function (e.g., testes). Indeed, studies in Macrostomum have shown interspecific variation in sex allocation towards the male and female functions, such as testes and ovaries (Singh et al, 2020b;Brand et al, 2022a;Singh & Schärer, 2021). This interspecific variation could potentially relate to the mating behaviour, as we can expect species that have a longer mating duration or higher mating frequency to have larger testes, if longer and/or more frequent mating implies that more sperm are transferred (Janicke & Schärer, 2009).…”

“…the amount of resources allocated to the male and female function) (van Velzen et al, 2009;Schärer & Pen, 2013). Indeed, studies have documented both inter-and intra-specific variation in sex allocation in Macrostomum (Singh et al, 2020b;Brand et al, 2022a;Singh & Schärer, 2021), with mating behaviour predicting the evolution of a species' sex allocation (Brand et al, 2022a), but not the evolution of its sex allocation plasticity (Singh & Schärer, 2021).…”