Meiosis is essential for the fertility of most eukaryotes and its structures and progression are conserved across kingdoms. Yet many of its core proteins show evidence of rapid or adaptive evolution. What drives the evolution of meiosis proteins? How can constrained meiotic processes be modified in response to challenges without compromising their essential functions? In surveying the literature, we find evidence of two particularly potent challenges to meiotic chromosome segregation that probably necessitate adaptive evolutionary responses: whole genome duplication, and abiotic environment, especially temperature. Evolutionary solutions to both kinds of challenge likely involve modification of homologous recombination and synapsis, probably via adjustments of core structural components important in meiosis I. Synthesizing these findings with broader patterns of the evolution of meiosis genes suggests that the structural components of meiosis co-evolve as adaptive modules and may change in primary sequence and function while maintaining three-dimensional structures and protein interactions. The often sharp divergence of these genes among species likely reflects periodic modification of entire multiprotein complexes driven by genomic or environmental changes. We suggest that the pressures that cause meiosis to evolve to maintain fertility may cause pleiotropic alterations of global crossover rates. We highlight several important areas for future research.