Asexual Adaptation Drives Transient and Reversible Changes in Mating Efficiency

The evolution of reproductive isolation is central to speciation, yet the earliest stages of this process remain poorly understood. In particular, it is unclear how rapidly barriers to mating arise during adaptation, whether they accumulate predictably, and how they depend on ecological context. Here, we investigate the evolution of mating efficiency during prolonged asexual adaptation in diploid Saccharomyces cerevisiae . Twelve replicate populations were evolved for 1200 generations in two distinct carbon environments, glucose and galactose, under strictly asexual conditions. At regular intervals, we induced sporulation and quantified mating efficiency using three complementary assays: within-population crosses, crosses between populations evolved in different environments, and crosses between evolved populations and the ancestral strain. We find that mating efficiency evolves during asexual adaptation, with outcomes that depend strongly on the environment. While glucose-evolved populations remain largely stable, galactose-evolved populations exhibit a reversible decline. Overall, changes in mating efficiency are dynamic, heterogeneous, and often transient, with evidence for both intrinsic reductions in mating competence and context-dependent incompatibilities between populations. Together, these results show that asexual adaptation can generate rapid but non-monotonic changes in mating compatibility. Early reductions in mating efficiency are heterogeneous, environment-dependent, and often reversible, and do not accumulate into stable reproductive isolation over the timescale examined. Our findings suggest that the initial stages of divergence are characterized by dynamic and contingent perturbations of reproductive traits, rather than a steady progression toward speciation.