Convergent evolution, the repeated evolution of similar phenotypes in independent lineages, can be caused by mutations at different genes, independent mutations at the same genes, and/or the repeated fixation of the same alleles. However, little is yet known about which mechanisms were prevalent in nature. Convergent reduction of bony plates covering the lateral body surface in Gasterosteus and Pungitius stickleback fishes can offer good opportunities to answer this question. Repeated plate reduction in several G. aculeatus populations in North America and Europe is known to be caused by the repeated use of the same allele of Ectodysplasin-A gene (Eda). Here, we have found that independent mutations on Eda and its receptor, Edar, caused plate reduction in Japanese Gasterosteus. Population genomic analysis suggested that this may be partially due to the lack of gene flow from other populations. In contrast, plate reduction in P. sinensis was caused by independent mutations at Edar. Phylogenetic analysis showed that introgression or ancestral polymorphism of the shared allele caused plate reduction in other Pungitius species. Thus, our study showed that Eda and Edar are the hotspot genes for the convergent plate reductions in sticklebacks.