Sperm are haploid, but must be functionally equivalent to distribute alleles equally among progeny. Accordingly, gene products are shared through spermatid cytoplasmic bridges which erase phenotypic differences between individual haploid sperm. Here, we show that a large class of mammalian genes are not completely shared across these bridges. We term these genes “genoinformative markers” (GIMs) and show that a subset can act as selfish genetic elements that spread alleles unevenly through murine, bovine, and human populations. We identify evolutionary pressure to avoid conflict between sperm and somatic function as GIMs are enriched for testis-specific gene expression, paralogs, and isoforms. Therefore, GIMs and sperm-level natural selection may help explain why testis gene expression patterns are an outlier relative to all other tissues.
Microsatellite markers were developed and evaluated in Hevea brasiliensis, an important crop species producing natural rubber of commercial utility. Of eight microsatellite markers, four were found to be highly informative, amplifying a total of 19 alleles when evaluated against 27 cultivated Hevea clones/genotypes. Power of discrimination of the microsatellite loci was in the range of 0.62-0.89, with a mean of 0.76 indicating these microsatellites could be valuable genetic markers for diversity characterization. A combination of four microsatellite markers was successfully used to discriminate uniquely all the 27 Hevea clones and some clone-specific allelic profiles were generated. Crossspecies amplification of the markers developed in H. brasiliensis had also been demonstrated with two other Hevea species, H. benthamiana and H. spruceana, indicating a high degree of sequence homology at the flanking regions. Sequence analysis of the repeat region at the 3¢-UTR of the hydroxymethylglutaryl-coenzyme A reductase gene, containing clusters of AG repeats in 15 clones, revealed the existence of two alleles based on the repeat length polymorphisms. Homozygosity as well as heterozygosity for both the alleles had also been detected among the clones. Frequency of homozygotes for the smaller allele (allele-1) was found to be lower than the larger allele (allele-2) among the primary clones of H. brasiliensis.
11Mendel's first law dictates that alleles segregate randomly during meiosis and are dis-12 tributed to offspring with equal frequency, requiring sperm to be functionally independent 13 of their genetic payload. Developing mammalian spermatids have been thought to accom-14 plish this by freely sharing RNA from virtually all genes through cytoplasmic bridges, 15 equalizing allelic gene expression across different genotypes. Applying single cell RNA * Corresponding author: rfriedman@ohanabio.com sequencing to developing spermatids, we identify a large class of mammalian genes whose 17 allelic expression ratio is informative of the haploid genotype, which we call genoinforma-18 tive markers (GIMs). 29% of spermatid-expressed genes in mice and 47% in non-human 19 primates are not uniformly shared, and instead show a confident allelic expression bias 20 of at least 2-fold towards the haploid genotype. This property of GIMs was significantly 21 conserved between individuals and between rodents and primates. Consistent with the 22 interpretation of specific RNA localization resulting in incomplete sharing through cyto-23 plasmic bridges, we observe a strong depletion of GIM transcripts from chromatoid bodies, 24 structures involved in shuttling RNA across cytoplasmic bridges, and an enrichment for 25 3 UTR motifs involved in RNA localization. If GIMs are translated and functional in the 26 context of fertility, they would be able to violate Mendel's first law, leading to selective 27 sweeps through a population. Indeed, we show that GIMs are enriched for signatures of 28 positive selection, accounting for dozens of recent mouse, human, and primate selective 29 sweeps. Intense selection at the sperm level risks evolutionary conflict between germline 30 and somatic function, and GIMs show evidence of avoiding this conflict by exhibiting 31 more testis-specific gene expression, paralogs, and isoforms than expression-matched con-32 trol genes. The widespread existence of GIMs suggests that selective forces acting at the 33 level of individual mammalian sperm are much more frequent than commonly believed. 34 2 Author's summary 35Mendel's first law dictates that alleles are distributed to offspring with equal frequency, 36 requiring sperm carrying different genetics to be functionally equivalent. Despite a small 37 number of known exceptions to this, it is widely believed that sharing of gene products 38 through cytoplasmic bridges erases virtually all differences between haploid sperm. Here, 39 we show that a large class of mammalian genes are not completely shared across these 40 bridges, therefore causing sperm phenotype to correspond partly to haploid genotype. We 41 term these genes "genoinformative markers" (GIMs) and show that their identity tends 42 2 to be conserved from rodents to primates. Because some GIMs can link sperm genotype 43 to function, they can be thought of as selfish genetic elements which lead to natural se-44 lection between sperm rather than between organisms, a violation of Mendel's first ...
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