Haploid selection in animals

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Selection in the haploid phase is well known in plants, but it is often ignored in animals. Recent studies show that haploid selection acts on diploid loci in animals in several ways; for example, via gametic gene expression, genomic imprinting, X inactivation and selection on non-transcribed genomic regions in sperm. Although haploid selection probably affects only a small fraction of the genome, the number of loci involved might be several hundred or more. Haploid selection is expected to have important consequences at these loci for diverse phenomena, including antagonism between adaptation to either the diploid or the haploid phases, conflict between levels of selection and the evolution of sexually dimorphic recombination rates. The topic is ripe for development: refined data about which loci experience haploid selection would open the door to a variety of comparative approaches that could illuminate how diverse forms of selection mold patterns of genetic variation.

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Evidence for haploid selection

Providing conclusive proof of haploid selection is a more subtle challenge than it might seem. For example, a gene that is transcribed during the haploid phase does not necessarily experience haploid selection. It has long been known that some gene products are shared between developing sperm in mice, via cytoplasmic bridges [5], making the sperm phenotype for those loci effectively diploid [6] (Figure 1). Convincing evidence that a gene that is expressed in spermatids is haploid selected would

How many genes are under haploid selection in mice?

To date, the most detailed studies of haploid selection have been conducted on mice. Yet, even in this well studied system, there remains uncertainty surrounding the number of loci exposed to haploid selection. In spite of our inability to estimate reliably the number of haploid selected genes in mice, we can put limits on it. The data are summarized in Table 3.

At least 75 genes are haploid selected in mice: two genes (Tcr and Spam1) known to be expressed in but not shared between mouse

Evolutionary implications of haploid selection

What major consequences might haploid selection have for diploid loci in animals? The percentage of the genome exposed to haploid selection seems, at most, to be only a few percent, at least in mammals. Consequently, it seems improbable that traits that integrate the effects of loci throughout the genome (e.g. inbreeding depression) are strongly influenced by haploid selection.

However, haploid selection is likely to have important evolutionary implications for those loci on which it acts. Some

Conclusions

The sources of haploid selection, as described here, suggest directions for empirical research. These include estimating the fraction of gene products shared between haploid spermatids, examining gametic expression in non-mammalian animals and determining the extent to which non-transcribed DNA functions in sperm. Accomplishing these research objectives will provide a more refined picture of the percentage of haploid selected loci in animals and will enable us to better understand the impact of

Acknowledgements

We thank D. Charlesworth, D. Hall, T. Lenormand, and J. Shore for insightful discussions. We also thank S. Otto and three anonymous reviewers for comments about the article. This research was supported by National Science Foundation grants DEB-9973221 and EF-0328594 to M.K.

Glossary

Aneuploid:
having one or more missing or extra chromosomes.
Arrhenotoky (haplodiploidy):
a genetic system in which females are diploid (they develop from fertilized eggs) and males are haploid (they develop from unfertilized eggs).
Diploid:
an organism whose somatic cells carry pairs of homologous autosomes. The term can also be applied to a single locus or cell.
Epistatic interactions:
interactions between alleles at different loci that affect fitness.
Gamete:
a cell that fuses with another gamete to

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