Evolution of haploid selection in predominantly diploid organisms

Abstract

Diploid organisms manipulate the extent to which their haploid gametes experience selection. Animals typically produce sperm with a diploid complement of most proteins and RNA, limiting selection on the haploid genotype. Plants, however, exhibit extensive expression in pollen, with actively transcribed haploid genomes. Here we analyze models that track the evolution of genes that modify the strength of haploid selection to predict when evolution intensifies and when it dampens the "selective arena" within which male gametes compete for fertilization. Considering deleterious mutations, evolution leads diploid mothers to strengthen selection among haploid sperm/pollen, because this reduces the mutation load inherited by their diploid offspring. If, however, selection acts in opposite directions in haploids and diploids ("ploidally antagonistic selection"), mothers evolve to reduce haploid selection to avoid selectively amplifying alleles harmful to their offspring. Consequently, with maternal control, selection in the haploid phase either is maximized or reaches an intermediate state, depending on the deleterious mutation rate relative to the extent of ploidally antagonistic selection. By contrast, evolution generally leads diploid fathers to mask mutations in their gametes to the maximum extent possible, whenever masking (e.g., through transcript sharing) increases the average fitness of a father's gametes. We discuss the implications of this maternal-paternal conflict over the extent of haploid selection and describe empirical studies needed to refine our understanding of haploid selection among seemingly diploid organisms.

Keywords: antagonistic selection; evolutionary theory; haploid selection; pollen competition; sperm competition.

Fig. 1.

Evolution of the selective arena experienced by haploids. (A) When the degree of gametic selection is maternally controlled, evolution drives the level of selection in the haploid phase toward the ESS, $c^{\ast }$, given by the solid curves (dashed curves are repelling). As the deleterious mutation rate per antagonistic locus ($\mathrm{\Upsilon }$) rises along the x axis, selection favors higher levels of gametic selection among mothers. On the other hand, as ploidally antagonistic selection becomes stronger in the haploid phase (larger τ), mothers evolve to reduce the degree of gametic selection. (B) The resulting effects on the fitness load experienced by diploid offspring at the ESS. Diploid mean fitness is reduced both by recurrent mutations (“mutation load” in dark gray) and by ploidally antagonistic selection (light gray) as mutation rate $\mathrm{\Upsilon }$ increases. Because gametic selection eliminates deleterious mutations, the mutation load (dark gray) is much lower than it would be in the absence of gametic selection (dashed line). Nevertheless, the total diploid load (ploidally antagonistic and mutation load) is often higher at the ESS, because the degree of gametic selection is also shaped by fitness variation in haploids. Other parameters: $t=0.1$, $s^k=0.2$, $h^k=0.1$, ${\sigma }^k=-0.1$, ${\eta }^k=0.9$, for both sexes.

Fig. 2.

Evolution of maternal control when fathers provision. Paternal control selects for reduced haploid expression to the minimum level possible ($p_{\text{min}}$). (A) When fathers provide a lower proportion of haploid gene products (lower $p_{\text{min}}$), mothers respond by evolving higher levels of gametic selection, with the ESS level of gametic selection shown by solid curves. (No paternal provisioning, $p_{\text{min}}=1$, corresponds to the red curve in Fig. 1A.) (B) Alternatively, when mothers can manipulate the impact of paternal diploid transcripts on fertilization (e.g., by delaying fertilization), mothers evolve to maximize haploid expression when the mutation rate is sufficiently high (ESS $c^{\ast }=1$, solid curves), but not when $\mathrm{\Upsilon }$ is low. The fitness of gamete type l from $Aa$ fathers was set to $g_l\left(p_{\text{min}},c_{ij}\right)=1-c_{ij}t\hspace{0.17em}\left(1-{\left(1-{\iota }_l^x\right)}^{1/x}\right)$ in A and to $g_l\left(p_{\text{min}},c_{ij}\right)=1-t\hspace{0.17em}\left(1-{\left(1-{\iota }_l^x\right)}^{1/x}\right)$ in B, where ${\iota }_l$ measures the extent to which a gamete carrying allele l from a heterozygous father has a fitness similar to that of an a gamete from an $aa$ father (${\iota }_l=1$) vs. an A gamete from an $AA$ father (${\iota }_l=0$). Functions were chosen to correspond to a dominance coefficient of 0.1 in gametes with an equal abundance of A and a gene products: $x=2.25$, ${\iota }_a=1-{\iota }_A$, and ${\iota }_A=\left(1-p_{\text{min}}\right)/2$ (A) or ${\iota }_A=\left(1-c_{ij}\right)\left(1-p_{\text{min}}\right)/2$ (B). Other parameters: $t=0.1$, $s^k=0.2$, $h^k=0.1$, $\tau =0.2$, ${\sigma }^k=-0.1$, ${\eta }^k=0.9$, for both sexes.