Principles of the highly ordered arrangement of metaphase I bivalents in spermatocytes of Agrodiaetus (Insecta, Lepidoptera)

Abstract

We have investigated the nature of highly ordered bivalent arrangement in lepidopteran spermatocytes by analysing and comparing the patterns of bivalent distribution in intact metaphase I plates of 24 closely related species of the genus Agrodiaetus (Lycaenidae). The studied species greatly differed in haploid chromosome numbers (from n = 13 to n = 90) and in the structure of their karyotypes. We found that the larger the bivalent, the closer to the centre of the metaphase plate it was situated. In species with a high chromosome number and asymmetrical karyotype structure, the largest bivalent was located in the centre of the circular metaphase plate. Bivalents of equal size were approximately equidistant from the centre of the metaphase plate and formed concentric circles around the largest bivalent. These principles are diametrically different from those known in the majority of other animals and plants, in which the smallest elements of the chromosome set are situated in the centre of metaphase plate. The only exception from the above principles was observed in spermatocytes of A. surakovi which were heterozygous for reciprocal translocation involving two or three chromosome pairs. In addition to one large bivalent, the heterozygous cells had a multivalent, the size of which was comparable to or even exceeded that of the largest bivalentin the karyotype. In spite of thelarge size, the multivalent was always situated at the periphery of metaphase plate. This indicated that the chromosome size itself is not the only factor determining the bivalent position. We also found that the structure of the metaphase plate is fundamentally different in mitotic and meiotic cells of Agrodiaetus. In spermatogonial metaphase, chromosomes were tightly brought together, forming a dense compact disk, whereas during metaphase I of spermatocytes, all bivalents were clearly separated from each other, and the distance between adjacent bivalents varied from 0.4 to 1.5 microm. Based on the above findings, we proposed a model of bivalent distribution in the Lepidoptera. According to the model, during congregation in the prometaphase stage there is a centripetal movement of bivalents made by a force directed to the centre of the metaphase plate transverse to the spindle. This force is proportional to the kinetochore size of a particular bivalent. The Lepidoptera have a special near-holokinetic type of chromosome organisation. Therefore, large bivalents having large kinetochores are situated in the central part of metaphase plate. Another possible factor affecting the bivalent position is the interaction of bivalents with the cisternae of the membrane system compartmentalising the intraspindle space.