Estimating the fitness effect of deleterious mutations during the two phases of the life cycle: a new method applied to the root-rot fungus Heterobasidion parviporum

Abstract

Many eukaryote species including taxa such as fungi or algae have a lifecycle with substantial haploid and diploid phases. A recent theoretical model predicts that such haploid-diploid lifecycles are stable over long evolutionary time scales when segregating deleterious mutations have stronger effects in homozygous diploids than in haploids and when they are partially recessive in heterozygous diploids. The model predicts that effective dominance, a measure that accounts for these two effects, should be close to 0.5 in these species. It also predicts that diploids should have higher fitness than haploids on average. However, an appropriate statistical framework to conjointly investigate these predictions is currently lacking. In this study, we derive a new quantitative genetic model to test these predictions using fitness data of two haploid parents and their diploid offspring and genome-wide genetic distance between haploid parents. We apply this model to the root-rot basidiomycete fungus Heterobasidion parviporum, a species where the heterokaryotic (equivalent to the diploid) phase is longer than the homokaryotic (haploid) phase. We measured two fitness-related traits (mycelium growth rate and the ability to degrade wood) in both homokaryons and heterokaryons and we used whole-genome sequencing to estimate nuclear genetic distance between parents. Possibly due to a lack of power, we did not find that deleterious mutations were recessive or more deleterious when expressed during the heterokaryotic phase. Using this model to compare effective dominance among haploid-diploid species where the relative importance of the two phases varies should help better understand the evolution of haploid-diploid life cycles.\n\nArticle summary for Issue HighlightsMany eukaryote species including taxa such as fungi or algae spend a large portion of their life cycle as haploids and as diploids. Clergeot, Rode et al. derive a statistical model to test whether deleterious mutations have stronger effects in homozygous diploids than in haploids, whether they are partially recessive in heterozygous diploids and whether diploids have higher fitness than haploids on average. As an illustration, they use their model to study growth rate and the ability to degrade wood in the root-rot fungus Heterobasidion parviporum. Their model should help gaining further insights into the evolution of haploid-diploid life cycles.