Short tandem repeats on the Y-chromosome (Y-STRs) are common DNA polymorphisms useful for genetic genealogy, population and evolutionary genetics, human genetics, pathology and forensic sciences. It is important to identify all Y-STR variants and to have knowledge of Y-STR mutation rates in order to correctly estimate the time to the most recent common ancestor (tMRCA) between paternally related individuals. When capillary electrophoresis (CE) is performed to analyze genealogical pairs, Y-STR sequence variations remain hidden when the number of repeats is identical. These hidden variations could be due to parallel Y-STR changes or modifications (PM) that occur independently in different lineages leading to alleles with identical number of repeats. In this study, we detect for the first time twelve PM by analyzing 133 males (960 meiosis) in extended deep-rooting family pedigrees on 42 Y-STRs. These PM were observed in nine Y-STR loci with mutation rates of at least 5.94 × 10-3 per generation. Sequencing analysis made it possible to distinguish insertions/deletions in different repeat regions revealing the presence of two unique changes in three PM on rapidly mutating and complex Y-STRs DYS724-ab and DYS518. Sequencing unraveled more information concerning the identity of alleles, and increased allelic discrimination possibilities which is of great importance in population genetics and forensic analysis. Limiting the analysis to CE could lead to wrong ancestral allele assumptions, to false negative interpretations and to tMRCA underestimations. These observations highlight the importance and added value of sequencing analysis and suggest a shift in genotyping methods from CE to next generation sequencing.