The evolution of separate sexes from hermaphroditism is thought to have occurred independently many times, and may be linked to the evolution of sex chromosomes. Even though we have a good understanding of the theoretical steps in the evolution of sex chromosomes from a hermaphrodite ancestor, the initial stages are still hard to study in animals because many well-studied animal sex chromosome systems are old. We addressed this problem by experimentally selecting a hermaphrodite via sex-limited experimental evolution for several generations, simulating the early stages in the evolution of a sex chromosome. After 14 generations, a fitness assay revealed evidence of incipient sex role specialization in the female-selected lines, presumably reflecting the release from constraints usually imposed by selection on the other sex role. Importantly, however, this was not simply explained by morphology because testis and ovary sizes did not diverge among treatments. There was no evidence of a change in the male-selected lines. Our study shows that sex role specialization can occur rapidly as a result of sex-limited selection, which is consistent with genetic constraints between sex roles, and in line with the first predicted steps toward the evolution of a new sex chromosome system.
Keywords: Macrostomum lignano; evolution of separate sexes; experimental evolution; gonad size; sex chromosomes; sexual dimorphism.
Evolutionary biologists have developed detailed theories which attempt to explain the evolution of sex chromosomes and separate sexes. Unfortunately, testing these theories can be challenging, since most of the best-studied sex chromosome systems are many millions of years old. This makes it difficult to disentangle cause and effect during sex chromosome evolution. In this study, we have tried to re-create the origin of sex chromosome and separate sexes from a hermaphroditic ancestor within the laboratory. Our aim was to better understand early sex chromosome evolution in real time. For this, we carried out experimental evolution in the simultaneously hermaphroditic flatworm Macrostomum lignano. When it mates, this species both receives sperm from the partner, and donates sperm back. We developed a genetic marker-based selection protocol which allowed us to restrict the worms’ reproduction, so that the male-selected lines could only produce offspring through sperm, and the female-selected lines could only produce offspring through eggs. After 14 generations of selection, we found that individuals from the female-selected lines became better at laying eggs, but worse at fertilizing their partners. However, the difference did not seem to be explained by changes in gonad size, since there were no differences between male- and female-selected worms in testes or ovary size. These results show that sexual specialization may be possible to evolve on surprisingly short time scales.
© The Author(s) 2023. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).