Fitness Effects of Mutation Accumulation in a Natural Outbred Population of Wild Radish (Raphanus Raphanistrum): Comparison of Field and Greenhouse Environments

Abstract

Spontaneous deleterious mutation has been measured in a handful of organisms, always under laboratory conditions and usually employing inbred species or genotypes. We report the results of a mutation accumulation experiment with an outbred annual plant, Raphanus raphanistrum, with lifetime fitness measured in both the field and the greenhouse. This is the first study to report the effects of spontaneous mutation measured under field conditions. Two large replicate populations (N e ≈ 600) were maintained with random mating in the greenhouse under relaxed selection for nine generations before the field assay was performed and ten generations before the greenhouse assay. Each generation, every individual was mated twice, once as a pollen donor and once as a pollen recipient, and a single seed from each plant was chosen randomly to create the next generation. The ancestral population was maintained as seeds at 4 • C. Declines in lifetime fitness were observed in both the field (1.7% per generation; P = 0.27) and the greenhouse (0.6% per generation; P = 0.07). Significant increases in additive genetic variance for fitness were found for stems per day, flowers per stem, fruits per flower and seeds per fruit in the field as well as for fruits per flower in the greenhouse. Lack of significance of the fitness decline may be due to the short period of mutation accumulation, the use of outbred populations, or both. The percent declines in fitness are at the high end of the range observed in other mutation accumulation experiments and give some support to the idea that mutational effects may be magnified under harsher field conditions. Thus, measurement of mutational parameters under laboratory conditions may underestimate the effects of mutations in natural populations.

Simultaneous Estimation of Additive and Mutational Genetic Variance in an Outbred Population of Drosophila serrata

“…On average, 5% of pairs failed to contribute offspring to the next generation; when pairs failed to produce any offspring, three offspring from some (randomly chosen) families were used to ensure that the census population size remained constant (240 pairs). Failure to reproduce might reflect viability selection; similarly low levels of reproductive failure were reported from a MCN experiment in radishes, where 3% of plants failed to produce seeds (Roles and Conner 2008), and in D. melanogaster, where 1-2% of pairs failed to reproduce each generation (Shabalina et al 1997).…”

“…In particular, direct estimation of the mutational variance from MCN experiments in the presence of substantial genetic variance in the base population has been highlighted as a key limitation of this design (Lynch et al 1999). One approach to solving this problem has been to impose a quantitative genetic breeding design simultaneously in both the MCN population and the ancestral population from which the MCN was initially derived and using these data to demonstrate higher genetic variance (owing to new mutations) in the MCN population (Roles and Conner 2008). The logistical challenge of applying a large quantitative genetic breeding design in two populations with a single generation (common environment) is likely to limit the application of MCN designs used in this way despite their benefit in terms of allowing the estimation of mutational variance in seminatural populations undergoing random mating and recombination.…”

Quantifying natural seasonal variation in mutation parameters with mutation accumulation lines

“…Whether a mutation is neutral, beneficial, or deleterious can vary across spatial and temporal environments or with environmental quality (Hietpas, Bank, Jensen, & Bolon, 2013; Kraemer, Morgan, Ness, Keightley, & Colegrave, 2016; Latta et al., 2015; Martin & Lenormand, 2006, 2015). Unfortunately, except for a very few studies (Roles & Conner, 2008; Roles, Rutter, Dworkin, Fenster, & Conner, 2016; Rutter, Shaw, & Fenster, 2010; Rutter et al., 2012) we have a relatively poor understanding of the effect of mutation on fitness under natural conditions and thus few direct measures of the temporal and spatial variability in mutation rates and effects outside of the laboratory.…”

Measurements of spontaneous rates of mutations in the recent past and the near future

“…(b) Measuring the fitness impact of accumulating mutations Measuring the fitness effect of mutations accumulating over time in a laboratory population under relaxed or absent selection has been a popular choice for estimating the rate of deleterious mutation (Mukai 1964;Mukai et al 1972;Charlesworth et al 1990Charlesworth et al , 1994Kondrashov & Houle 1994;Fernández & López-Fanjul 1996;Kibota & Lynch 1996;Keightley & Caballero 1997;Schultz et al 1999;Loewe et al 2003;Charlesworth et al 2004;Houle & Nuzhdin 2004;Gong et al 2005a,b;Roles & Conner 2008). Starting from an inbred population, it is possible to measure the impact on fitness of many mutations that have accumulated over dozens of generations.…”