This study followed the typical and atypical pathways of spermatogenesis in Venustaconcha ellipsiformis (Conrad, 1836) (Bivalvia: Unionoida: Unionidae), during an entire year and documents the developmental stages of both using light and transmission electron microscopy. The spermatozoa produced by both pathways were essentially morphologically identical and contained a single acrosomal vesicle. Production of spermatozoa in the two pathways overlapped from May to October, and vitellogenic eggs were present over this same time period. Atypical spermatogenesis also occurred from November through April. The typical pathway involved the mitotic and meiotic divisions that include spermatogonial cells, primary and secondary spermatocytes, spermatids and mature spermatozoa. In contrast, atypical spermatozoa appeared to be produced in a pathway that included spermatozoa morulae and spermatids produced from spermatogonial cells located in Sertoli cells. Large amorphous inclusions (Al) observed in Sertoli cells, and apparently acting as secondary lysosomes in digesting morulae, are described for the first time. The morphology of the Al was variable, with the Al sometimes containing structures that were organelle-like in appearance and some of the Al appeared to merge together. Phagocytes associated with both the typical and atypical pathways, but distinct from Sertoli cells, were observed clearing the acini of cellular debris. Immunoelectron microscopy detected the presence of both female-transmitted (F) and male-transmitted (M) mitochondria in the spermatozoa present in July (when fertilization takes place). We propose that the necessity of producing spermatozoa with F and M mt genome-bearing mitochondria, to maintain dioecy and 50 : 50 sex ratios in freshwater bivalve populations, accounts for the > 200 million year maintenance of two spermatogenic pathways in the Unionoida.