Hybrid breakdown is temporary and not expressed in a novel environment during 50 generations of experimental evolution in Tetranychus urticae hybrids

Hybridization, the interbreeding between species or genetically distinct populations, can lead to deleterious fitness consequences, but simultaneously it can boost adaptive potential by increasing genetic variation, especially in novel environments. However, how incompatibilities and beneficial genetic combinations interplay across generations remains poorly understood. Here, we tracked how two fitness proxies, the absolute number of adult offspring and the proportion of eggs that reached adulthood, evolve in parental and hybrid populations at three different time points over 50 generations, in both novel and ancestral environments. To test this, we used two geographically distinct populations with low divergence (Dxy=0.002) of the two-spotted spider mite (Tetranychus urticae). Across the first three generations, hybrids showed significantly lower fitness than parental populations in the ancestral environment, indicating incompatibilities between the parental genomes. In contrast, hybrid and parental fitnesses were similar in the novel environment, indicating that the impact of incompatibilities was minor compared to the selection imposed by the novel environment. However, after 50 generations, hybrids displayed similar fitness relative to parental populations in all environments, suggesting resolution of the incompatibilities. Furthermore, around generation 45, hybrids temporarily outperformed parental populations in a novel environment, suggesting a transient window of higher adaptive potential, before fitness stabilized again by generation 50. In conclusion, we show that hybrid populations of T. urticae can swiftly purge incompatibilities when genetic divergence is low. These findings suggest that the dynamics of incompatibility resolution and adaptive potential of novel haplotypes play out over a long time frame, highlighting the importance of tracking hybrid fitness past the first few generations.