“Haploid Selection in Animals: Exploring the Fitness Consequences and Underlying Mechanisms”, 2018-08-24 (; backlinks; similar):
A consequence of sexual reproduction in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid gametic phases. While our focus in evolutionary biology is on selection during the diploid phase, we know relatively little about selection occurring during the haploid gametic stage. This is particularly true in predominantly diploid animals, where gene expression and hence selection have long been thought to be absent in haploid cells like gametes and particularly sperm.
During my PhD, I tested the idea of selection during the haploid gametic phase using zebrafish Danio rario as a study species. I combined a large-scale selection experiment over 3 generations with fitness assays and next-generation sequencing to assess the importance of haploid selection. We measured offspring fitness in all 3 generations. In addition, we compared gene expression in brain and testes of F1 and F3 adult male from each treatment by RNA sequencing.
We found that offspring sired by longer-lived sperm showed higher survival rate and higher early-life and late-life reproductive fitness compared to offspring sired by shorter-lived sperm. We also found differentially expressed genes between the 2 treatments with functions in metabolic and developmental pathways.
These findings suggest that the observed fitness differences to be caused by small expression changes in many basic genes. We also tested for a genetic underpinning of the selected sperm phenotypes and identified allelic differences across the entire genome. Finally, we investigated the additive genetic component and parental effect of different sperm phenotypes. We found generally low additive genetic variation and high parental effects on sperm performance traits.
In conclusion, this thesis provides evidence that the phenotypic variation among intact fertile sperm within an ejaculate affects offspring fitness throughout life and provides a clear link between sperm phenotype and offspring fitness and between sperm phenotype and sperm genotype.
[Keywords: sperm, evolution, haploid selection, reproductive aging, fitness]
…List of Papers: This thesis is based on the following papers, which are referred to in the text by their Roman numerals.
I. et al 2017, “Sperm selection within a single ejaculate increases offspring fitness” II. Alavioon et al, “Within-ejaculate selection for sperm longevity reduces male reproductive ageing”. Manuscript III. Alavioon et al, “The fitness consequences of selection in haploid sperm across generations”. Manuscript IV. Alavioon et al, “Sperm performance traits exhibit low heritability and strong parental effects in external fertilizer”. Manuscript.
Additional Papers:
The following papers were published/in publishing process during the course of my doctoral studies but are not part of the thesis.
et al 2014, “Sperm variation within a single ejaculate affects offspring development in Atlantic salmon”
et al 2014, “Evolution of differential maternal age effects on male and female offspring development and longevity”
et al 2017, “No evidence for MHC class II-based disassortative mating at the gamete level in Atlantic salmon”
Silva et al, “Perceived sperm competition intensity in zebrafish males affects gene expression in early offspring”. Manuscript
…The mechanisms and outcomes of selection occurring during diploid and haploid phases differ substantially (1965). Because diploids have 2 copies of each allele, they can mask recessive mutations, which are therefore less exposed to selection. In contrast, when an allele is expressed in a haploid state, it is entirely exposed to selection since there is no masking effect of a sister allele. This can in fact facilitate the rate of spreading and fixation of beneficial alleles while reducing the accumulation of deleterious mutations in a population by efficiently eliminating deleterious mutations (1924; 1965; 1998). …Haploid selection is a situation in which a phenotype under selection is determined by a haploid allele (2004).
…in animals, haploid selection is understudied due to an existing dogma that gene expression at the post-meiotic haploid phase is largely absent. Many researchers dismissed the possibility of haploid selection in animals for several reasons. The first reason was the fact that most animals spend the majority of their life cycle as diploids followed by a very short haploid stage. The other reason was that the DNA in sperm/gametes is densely packed and almost entirely lacking a cytoplasm, therefore haploid gene expression and translation (1976) are impossible and sperm in basically transcriptionally silent (1999; 2004). Although later on, researchers found evidence of post-meiotic DNA transcription in sperm, they believed that the newly made transcriptomic products and other molecules could be shared between sperm cells through cytoplasmic bridges (2004), therefore, all sperm cells benefit from the similarly defined sperm traits and none of the sperm develops advantages over others. Later on researchers found more proofs of DNA transcription ( et al 1981) and even small amounts of protein translation in sperm cells (2006; 2007; 2008), and evidence that showed not all of the transcriptomes and proteins can be passed through cytoplasmic bridges (). They also found that the alterations of the epigenome of sperm after meiosis ( et al 2016) cause individual sperm to vary and to affect the next generation offspring differently. All these post-meiotic changes may form a basis for differences between individual sperm and create a potential for haploid selection to occur. In 2004 a review on a few studies showed several loci in animals’ genome experience haploid selection and it emphasized that such selection might potentially affect several evolutionary processes. Antagonistic adaptation between haploid and diploid phases, sex specific recombination rates and genome imprinting, loads of deleterious mutations and extent of inbreeding depression are a few, among the many ways that haploid selection can affect evolutionary processes (1987; et al 1993; 2004; 2013).