The present fine structure study deals with the behavior of the mitochondria during meiosis I in males of a leaf beetle, Agelastica alni. For the sake of completeness, the restructuring of cytoplasmic elements, spindles, and nuclei is also described. Serial ultrathin sections through prophase I spermatocytes in diverse developmental stages and metaphase and telophase I spermatocytes were studied. While mitochondria were scattered throughout the cytoplasm in pachytene, they aggregated in the vicinity of the nucleus in diplotene and formed prominent stacks. It was clear that individual mitochondrial stacks were interconnected by elongated mitochondria, but the three-dimensional relationship of mitochondria within the stacks was difficult to assess on account of their dense packing. Filamentous and granular material was found between the individual mitochondria and may link them. In diakinesis, the stacks gave rise to elongated mitochondria located in invaginations of the nuclear envelope. When the nuclear envelope opened in prometaphase I, some mitochondria entered the spindle area but the majority of them remained lateral to the forming spindle apparatus. Spindles in metaphase I spermatocytes were characterized by a spindle envelope consisting of two closely neighboring cisternae of smooth endoplasmic reticulum and some elongated mitochondria inside this sheath. The bulk of the mitochondria was arranged at the cytoplasmic face of the spindle envelope. Telophase cells possessed elongated mitochondria oriented parallel to the spindle apparatus. A volumetric approach showed that the entire mitochondrial mass of prophase I spermatocytes associated with the spindle apparatus in metaphase I. The close association of mitochondria with the spindle apparatus may guarantee roughly bisection of the chondriome during meiotic division. The association between mitochondria and prophase I nuclei may be a preparatory step for the imminent alignment with the spindle but my also serve the high energy demands of the nuclear compartment in this system. (C) 1996 Academic Press, Inc.