Lamarckian inheritance has been largely discredited until the recent discovery of transgenerational epigenetic inheritance. However, transgenerational epigenetic inheritance is still under debate for unable to rule out DNA sequence changes as the underlying cause for heritability. Here, through profiling of the sperm methylomes and genomes of two recently diverged rat subspecies, we analyzed the relationship between epigenetic variation and DNA variation, and their relative contribution to evolution of species. We found that only epigenetic markers located in differentially methylated regions (DMRs) between subspecies, but not within subspecies, can be stably and effectively passed through generations. DMRs in response to both random and stable environmental difference show increased nucleotide diversity, and we demonstrated that it is variance of methylation level but not deamination caused by methylation driving increasing of nucleotide diversity in DMRs, indicating strong relationship between environment-associated changes of chromatin accessibility and increased nucleotide diversity. Further, we detected that accelerated fixation of DNA variants occur only in inter-subspecies DMRs in response to stable environmental difference but not intra-subspecies DMRs in response to random environmental difference or non-DMRs, indicating that this process is possibly driven by environment-associated fixation of divergent methylation status. Our results thus establish a bridge between Lamarckian inheritance and Darwinian selection.

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