Intraspecific Variation in the Rates of Mutations Causing Structural Variation in Daphnia magna

Abstract

Mutations that cause structural variation are important sources of genetic variation upon which other evolutionary forces can act, however they are difficult to observe and therefore few direct estimates of their rate and spectrum are available. Understanding mutation rate evolution, however, requires adding to the limited number of species for which direct estimates are available, quantifying levels of intraspecific variation in mutation rates, and assessing whether rate estimates co-vary across types of mutation. Here, we report structural variation-causing mutation rates (svcMRs) for six categories of mutations (short insertions and deletions, long deletions and duplications, and deletions and duplications at copy number variable [CNV] sites) from 9 genotypes of Daphnia magna collected from three populations in Finland, Germany, and Israel using a mutation accumulation approach. Based on whole genome sequence data and validated using simulations, we find svcMRs are high (2 orders of magnitude higher than base substitution mutation rates measured in the same lineages), highly variable among populations, and uncorrelated across categories of mutation. Furthermore, to assess the impact of scvMRs on the genome, we calculated rates while adjusting for the lengths of events and ran simulations to determine if the mutations occur in genic regions more or less frequently than expected by chance. Our results pose a challenge to most prevailing theories aimed at explaining the evolution of the mutation rate, underscoring the importance of obtaining additional mutation rate estimates in more genotypes, for more types of mutation, in more species, in order to improve our future understanding of mutation rates, their variation, and their evolution.

Low spontaneous mutation rate in a complex multicellular eukaryote with a haploid-diploid life cycle

“…2014; Liu and Zhang 2019), Daphnia (Keith et al . 2016; Ho and Schaack 2021) and Caenorhabditis elegans (Konrad et al . 2018).…”

“…for only few species such as green algae (Leger-Pigout and Krasovec 2022), yeast (Lynch et al 2008;Zhu et al 2014;Liu and Zhang 2019), Daphnia (Keith et al 2016;Ho and Schaack 2021) and Caenorhabditis elegans (Konrad et al 2018). Structural mutations are evolutionarily important as they impact a large portion of the genome and may originate major adaptations.…”

Very small spontaneous structural mutation rate in green algae

“…This hypothesis is the most accepted to explain the mutation rate variation between species, even if other factors impact it but with smaller effect such as GC content (Krasovec et al ., 2017), genome size, generation time or metabolic rate (Martin & Palumbi, 1993; Mooers & Harvey, 1994; Thomas et al ., 2010; Weller & Wu, 2015). Both µ bs and µ id depends so mostly of N e , but our knowledge about the spontaneous structural mutation rate µ st is very poor (Press et al ., 2019; Ho & Schaack, 2021) and available in only few models (see Table 3 of Katju and Bergthorsson 2019 for copy number variant for example). Structural mutations, defined here as duplications, large insertions-deletions, inversions or chromosome rearrangements, may have stronger phenotypic effect than nucleotide and short indels mutations because they impact a larger portion of the genome.…”

High rates of spontaneous chromosomal duplications unravel dosage compensation by translational regulation

“…Whole chromosome duplications detected here are part of structural mutations, such as large insertions-deletions, inversions or chromosome rearrangements and may have huge phenotypical effect, much more than a nucleotide or short insertion-deletion mutations because they impact a larger proportion of the genome. However, studies on the structural mutation rate are very limited (Press et al 2019; Ho and Schaack 2021) making this study a significant step in our understanding of structural mutation rate in unicellular eukaryote. We then estimate the effect of such chromosome duplication on the transcription and translation rates by coupling transcriptomics with translatomics sequencing in one cryopreserved mutation accumulation line of Bathycoccus prasinos .…”