Determinants of rapid adaptation in species with large variance in offspring production

The speed of population adaptation to changing biotic and abiotic environments is determined by the interaction between genetic drift, positive selection and linkage effects. Many marine species (fish, crustaceans), invertebrates and pathogens of humans and crops, exhibit sweepstakes reproduction characterized by the production of a very large amount of offspring (fecundity phase) from which only a small fraction may survive to the next generation (viability phase). Using stochastic simulations, we investigate whether the occurrence of sweepstakes reproduction affects the efficiency of a positively selected unlinked locus, and thus, the speed of adaptation since fecundity and/or viability have distinguishable consequences on mutation rate, probability and fixation time of advantageous alleles. We observe that the mean number of mutations at the next generation is always the function of the population size, but the variance increases with stronger sweepstakes reproduction when mutations occur in the parents. On the one hand, stronger sweepstakes reproduction magnifies the effect of genetic drift thus increasing the probability of fixation of neutral allele and decreasing that of selected alleles. On the other hand, the time to fixation of advantageous (as well as neutral) alleles is shortened by stronger sweepstakes reproduction. Importantly, fecundity and viability selection exhibit different probabilities and times to fixation of advantageous alleles under intermediate and weak sweepstakes reproduction. Finally, alleles under both strong fecundity and viability selection display a synergistic efficiency of selection. We conclude that measuring and modelling accurately fecundity and/or viability selection are crucial to predict the adaptive potential of species with sweepstakes reproduction.

Automated summary

The speed of population adaptation is influenced by genetic drift, positive selection, and linkage effects. Sweepstakes reproduction, common in many marine species and pathogens, can affect the efficiency of positive selection and the speed of adaptation due to its consequences on mutation rate, probability, and fixation time of advantageous alleles. Stronger sweepstakes reproduction increases the variance of mutations, amplifies the effect of genetic drift, shortens fixation time for advantageous alleles, and exhibits different probabilities and times to fixation under different selection pressures. Accurately measuring and modeling sweepstakes reproduction is crucial for predicting adaptive potential.