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Evolution of haploid selection in predominantly diploid organisms
Sunday, 2016/01/03 | 06:55:28
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Sarah P. Otto, Michael F. Scott, and Simone Immler
EVOLUTION
Significance
Predominantly diploid organisms shape the extent to which their haploid gametes and gametophytes experience selection. Although animals are thought to experience only mild selection in the haploid stage, plants often experience strong haploid selection. When should parents limit exposure of gametes to haploid selection and when should they strengthen this selection? We develop mathematical models that consider the “selective arena” within which male gametes or gametophytes (sperm or pollen) compete for fertilization, examining how the intensity of this selective arena evolves when controlled by the mother or the father. These models predict substantial variation in the outcome, depending on whether mothers or fathers exert more control over the selective arena, with mothers often favoring stronger haploid selection than fathers.
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.
See http://www.pnas.org/content/112/52/15952.abstract.html?etoc PNAS December 29 2015; vol. 112, no. 22: 15952–15957
Fig. 2. Evolution of maternal control when fathers provision. Paternal control selects for reduced haploid expression to the minimum level possible (pmin). (A) When fathers provide a lower proportion of haploid gene products (lower pmin), mothers respond by evolving higher levels of gametic selection, with the ESS level of gametic selection shown by solid curves. (No paternal provisioning, pmin=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∗=1, solid curves), but not when Υ is low. The fitness of gamete type l from Aa fathers was set to gl(pmin,cij)=1−cijt (1−(1−ιxl)1/x) in A and to gl(pmin,cij)=1−t (1−(1−ιxl)1/x) in B, where ιl 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 (ιl=1) vs. an A gamete from an AA father (ιl=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, ιa=1−ιA, and ιA=(1−pmin)/2 (A) or ιA=(1−cij)(1−pmin)/2 (B). Other parameters: t=0.1, sk=0.2, hk=0.1, τ=0.2, σk=−0.1, ηk=0.9, for both sexes. |
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