Evolution of sex allocation plasticity in a hermaphroditic flatworm genus

Abstract

Sex allocation theory in simultaneous hermaphrodites predicts that optimal sex allocation is influenced by local sperm competition, which occurs when related sperm compete to fertilize a given set of eggs. Different factors, including the mating strategy and the ability to self-fertilize, are predicted to affect local sperm competition and hence the optimal SA. Moreover, since the local sperm competition experienced by an individual can vary temporally and spatially, this can favour the evolution of sex allocation plasticity. Here, using seven species of the free-living flatworm genus Macrostomum, we document interspecific variation in sex allocation, but neither their mating strategy nor their ability to self-fertilize significantly predicted sex allocation among these species. Since we also found interspecific variation in sex allocation plasticity, we further estimated standardized effect sizes for plasticity in response to (i) the presence of mating partners (i.e. in isolation vs. with partners) and (ii) the strength of local sperm competition (i.e. in small vs. large groups). We found that self-fertilization predicted sex allocation plasticity with respect to the presence of mating partners, with plasticity being lower for self-fertilizing species. Finally, we showed that interspecific variation in sex allocation is higher than intraspecific variation due to sex allocation plasticity. Our study suggests that both sex allocation and sex allocation plasticity are evolutionarily labile, with self-fertilization predicting the latter in Macrostomum.

Keywords: hypodermic insemination; local mate competition; phenotypic plasticity; reciprocal mating; self-fertilization; sperm competition.

FIGURE 1

(a) A visualization of our hypotheses for the effect of the number of available social mates on the predicted sex allocation for species that either obligatorily outcross (red), species that both self‐fertilize and outcross simultaneously (blue), or species that obligatorily self‐fertilize (grey). The shown estimate of sex allocation is based on testis size / (testis size + ovary size) so that larger sex allocation values represent more strongly male‐biased allocation. As the number of social mates increases, the so‐called mating group size (MGS, i.e. the number of actual mates plus one) is expected to increase, whereas the level of local sperm competition (LSC) is expected to decrease. Note that for species that obligatorily self‐fertilize, MGS always remains one and LSC is always maximal, leading to a highly female‐biased sex allocation (i.e. the minimal male allocation to allow for full self‐fertility), independently of the number of social mates (indicated by grey dot and stippled line). For species that both self‐fertilize and outcross simultaneously, the MGS is already increased when the number of mates is one, since own sperm will compete with the partner's sperm. Also, in species that outcross only, the prediction of when the number of mates is one is only the minimal male allocation to allow for full outcross fertility. Note that these SA predictions are only approximate, since the degree to which MGS increases with the number of social mates will likely vary, and the extent of self‐fertilization and outcrossing is unclear in the species that show both. (b) Photograph and schematic drawing of an adult Macrostomum cliftonense (total length ~1.2 mm), showing the typical location of testes and ovaries (and the eggs formed from the ovaries)

FIGURE 2

Effect of group size on estimates of sex allocation in seven different Macrostomum species (given by different colours). The line types represent the two mating strategies, and the symbols represent the ability to self‐fertilize. The plots show means and 95% confidence intervals of the raw (untransformed) data. The data have been jittered along the x‐axis to decrease overlap. Note that for M. lignano, data from seven independent experiments are shown

FIGURE 3

Standardized SA plasticity effect sizes for the effect of the presence of mating partners (i.e. comparing isolated worms vs. worms with partners) and the strength of local sperm competition (i.e. comparing worms in pairs vs. octets) among seven Macrostomum species (right side). The error bars represent 95% confidence intervals. For M. lignano, data from multiple experiments are shown. Also indicated is whether self‐fertilization (P. Singh, personal observations) or/and reciprocal mating behaviour (Singh et al., 2022) is present or absent in a species (left side), and these traits are mapped onto a trimmed maximum‐likelihood phylogeny of the genus (i.e. the H‐IQ‐TREE phylogeny from Brand et al., , which is based on 385 genes in 98 Macrostomum species), and all the shown bipartitions in this tree had maximal support, as indicated by ultrafast bootstrap support (first number) and approximate likelihood‐ratio tests (second number), respectively. A and B represent the inferred ancestral states at important internal nodes, suggesting that there are independent origins of hypodermic insemination and self‐fertilization in the genus (see also Methods and Figure S1 for details)