Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition

Abstract

Sex allocation theory predicts the optimal allocation to male and female reproduction in sexual organisms. In animals, most work on sex allocation has focused on species with separate sexes and our understanding of simultaneous hermaphrodites is patchier. Recent theory predicts that sex allocation in simultaneous hermaphrodites should strongly be affected by post-copulatory sexual selection, while the role of pre-copulatory sexual selection is much less clear. Here, we review sex allocation and sexual selection theory for simultaneous hermaphrodites, and identify several strong and potentially unwarranted assumptions. We then present a model that treats allocation to sexually selected traits as components of sex allocation and explore patterns of allocation when some of these assumptions are relaxed. For example, when investment into a male sexually selected trait leads to skews in sperm competition, causing local sperm competition, this is expected to lead to a reduced allocation to sperm production. We conclude that understanding the evolution of sex allocation in simultaneous hermaphrodites requires detailed knowledge of the different sexual selection processes and their relative importance. However, little is currently known quantitatively about sexual selection in simultaneous hermaphrodites, about what the underlying traits are, and about what drives and constrains their evolution. Future work should therefore aim at quantifying sexual selection and identifying the underlying traits along the pre- to post-copulatory axis.

Figure 1.

Basic elements of sex allocation theory for hermaphrodites. (a) Unequal male (grey) and female (white) material contribution to the zygote or offspring (assuming no paternal care). (b) Equal male and female genetic contribution to the zygote or offspring (the Fisher condition). (c) Effect of the number of competing hermaphrodites (i.e. mating group size minus unity) on the optimal sex allocation (note that self-fertilizing individuals should be counted as mates, as their sperm can potentially compete with that of a partner). (d) Under random mating and in large populations optimal male and female allocation are equal (balanced or Fisherian sex allocation). (e) With smaller numbers of competing hermaphrodites the optimal sex allocation is increasingly female-biased.

Figure 2.

Logic of the relationships explored in the text and the model. (a) We assume that the total reproductive allocation is partitioned into female allocation, f, which we assume to yield linear fitness returns (depicted in (c)), and male allocation consisting of a pre-copulatory trait, q, a post-copulatory trait, p, and sperm production, r (we do not imply that the visualized quantities are necessarily representative of a specific biological scenario). (b) Now imagine that a sperm recipient mates n₀ = 5 times. Assuming fair raffle sperm competition, we expect all five sperm donors to contribute equally to the sperm stored in a sperm recipient (top), leading to a number of mates of n = 5, unless the pre-copulatory trait, q, leads to an increase in the number of mates (indicated by arrow (1) and depicted in (d)). Owing to the action of the post-copulatory trait, p (indicated by arrow (2) and depicted in (e)) and possibly additional stochastic events, the contributions to the sperm stored in a sperm recipient can become highly skewed (the depicted example assumes no stochastic events and that allocation to p leads to a displacement of two thirds of the previously stored sperm). This results in a much lower effective number of mates, n_e ≈ 2, than expected under fair-raffle sperm competition, and thus a much lower optimal male allocation to sperm production, r (indicated by arrow (3) and depicted in (f)) (i.e. because the fitness gain curve for sperm production saturates more quickly with smaller n). Note that the parameters c and a scale the effects of parameters q and p, respectively.

Figure 3.

Relationship between the (nominal) number of mates, n, and the effective number of mates, n_e. (a) Effect assuming a beta distribution for the paternity share, without (a = 0) or with (a = 2) an effect of the post-copulatory trait, p, on ejaculate size, and with a small (b = 1) or large (b = 2) effect of p on the variance of the beta distribution. (b,c) Effect of different sperm precedence patterns as a function of different P₂-values.

Figure 4.

Relationship between the number of mates, n, and the allocation towards the pre-copulatory trait, q, the post-copulatory trait, p, the sperm production, r and the total male allocation (sum of q, p and r) for four different scenarios that we have explored in the model. In all panels the red, light blue and dark blue lines are for values of parameter a = 0, 1, and 2, respectively, and the solid versus dashed lines are for different values of other parameters explored in each scenario. (a) Scenario 1: nominal number of mates (n, assuming fair raffle sperm competition, solid lines) versus effective number of mates (n_e, assuming basic random paternity skews, dashed lines) (for b = 0 and c = 0). (b) Scenario 2: small (b = 1, solid lines) versus large (b = 2, dashed lines) effect of the post-copulatory trait, p, on the paternity skews (for c = 0). (c) Scenario 3: moderate (P₂ = 0.67, solid lines) versus strong (P₂ = 0.80, dashed lines) second male sperm precedence pattern (for b = 1 and c = 0). (d) Scenario 4: effect of the pre-copulatory trait, q, on the additional number of mates (for b = 1 and c = 5) (only cases where values of q > 0 evolve are shown, which requires large values of c and n).