The rapid evolution of a trait in a clade of organisms can be explained by the sustained action of natural selection or by a high mutational variance, that is the propensity to change under spontaneous mutation. The causes for a high mutational variance are still elusive. In some cases, fast evolution depends on the high mutation rate of one or few loci with short tandem repeats. Here, we report on the fastest evolving cell fate among vulva precursor cells in Caenorhabditis nematodes, that of P3.p. We identify and validate causal mutations underlying P3.p's high mutational variance. We find that these positions do not present any characteristics of a high mutation rate, are scattered across the genome and the corresponding genes belong to distinct biological pathways. Our data indicate that a broad mutational target size is the cause of the high mutational variance and of the corresponding fast phenotypic evolutionary rate.
Keywords: C. elegans; caenorhabditis; evolutionary biology; evolutionary rate; genetics; genomics; mutational target; mutational variance; vulva.
Heritable characteristics or traits of a group of organisms, for example the large brain size of primates or the hooves of a horse, are determined by genes, the environment, and by the interactions between them. Traits can change over time and generations when enough mutations in these genes have spread in a species to result in visible differences. However, some traits, such as the large brain of primates, evolve faster than others, but why this is the case has been unclear. It could be that a few specific genes important for that trait in question mutate at a high rate, or, that many genes affect the trait, creating a lot of variation for natural selection to choose from. Here, Besnard, Picao-Osorio et al. studied the roundworm Caenorhabditis elegans to better understand the causes underlying the different rates of trait evolution. These worms have a short life cycle and evolve quickly over many generations, making them an ideal candidate for studying mutation rates in different traits. Previous studies have shown that one of C. elegans’ six cells of the reproductive system evolves faster than the others. To investigate this further, Besnard, Picao-Osorio et al. analysed the genetic mutations driving change in this cell in 250 worm generations. The results showed that five mutations in five different genes – all responsible for different processes in the cells – were behind the supercharged evolution of this particular cell. This suggests that fast evolution results from natural selection acting upon a collection of genes, rather than one gene, and that many genes and pathways shape this trait. In conclusion, these results demonstrate that how traits are coded at the molecular level, in one gene or many, can influence the rate at which they evolve.
© 2020, Besnard et al.