Y-chromosome losses leading to XO sex chromosome systems are common in many male heterogametic groups (approximately 15% of examined species). However despite a clear understanding of how Y-chromosomes are expected to decay our understanding of why some lineages frequently lose Y-chromosomes while others do not is limited. The fragile Y hypothesis proposes that in species with chiasmatic meiosis the rate of Y-chromosome aneuploidy and the size of the recombining region have a negative correlation. The fragile Y hypothesis provides a number of novel insights not possible under traditional models of sex chromosome evolution. Specifically, as the recombining region of the sex chromosomes shrinks increased rates of Y aneuploidy will impose positive selection for 1) gene movement off the Y; 2) translocations and fusions which expand the recombining region; and 3) alternative meiotic segregation mechanisms (achiasmatic or asynaptic male meiosis). We have built a time-calibrated phylogeny for more than 1,000 beetles and have applied comparative methods to understand the tempo and mode of sex chromosome evolution in beetles with chiasmatic and achiasmatic male meiosis. We show that beetles with chiasmatic meiosis lose Y-chromosomes more frequently and that Y chromosome loss is associated with species that have on average smaller recombining regions. Likewise limited data from mammals is also consistent with Y aneuploidy being an important force in the evolution of sex chromosomes and meiotic mechanisms. This hypothesis and our analyses raise doubts about the long-term stability of the human Y-chromosome despite recent evidence for stable gene content in older nonrecombining regions.