Aberrant spermatogenesis and sex determination in Bourletiellidae (Hexapoda, Collembola), and their evolutionary significance

Light and electron microscopic evidence is provided to describe a new examp le of a postzygotic sex-determination system in two collembolan species, Bo urletiella arvalis and B. hortensis. In B. arvalis, where chromosome number could be assessed, both sexes are homogametic (n=6) and all zygotes have a n identical chromosome composition (2n=12). However, male embryos develop a fter the loss of two sex chromosomes, making the male genotype 2n=10 (4AAX( 1)0X(2)0). On the other hand, female embryos develop if the zygote retains all chromosomes and the female generic system is, therefore, 4FAAX(1)X(1)X( 2)X(2) (2n=12). As an apparent consequence of the lack of two chromosomes i n the male germ cells, spermatogenesis is aberrant. At the first meiotic di vision, in fact, the two resulting secondary spermatocytes receive a differ ent number of chromosomes: six and four. The cells which receive six chromo somes tone haploid set of four autosomes and two sex chromosomes) proceed t hrough the meiotic process and the two spermatids generated produce two spe rmatozoa by a normal spermiogenesis. The cells receiving only four chromoso mes do not undergo the second meiotic division and soon degenerate. The deg enerating cells can be considered a morphological marker for this process, as they are easily recognizable at the electron microscope from the functio nal secondary spermatocytes by the appearance of the nucleus (totally conde nsed), the reduction of the cytoplasm (limited to a thin layer surrounding the nucleus), and the lack of most cytoplasmic organelles (with the excepti on of a couple of centrioles). Electron microscopic evidence has been colle cted for both species, allowing to extend the same process to B. hortensis, even if chromosomes could not be counted in this species. Therefore, as a result of the spermatocyte elimination, the efficiency of spermatogenesis i s reduced to 50%. This process is identical to that observed in other colle mbolan species of the suborder Symphypleona, and it is suggested that it re presents a synapomorphic feature uniting the families Dicyrtomidae, Sminthu ridae and Bourletiellidae (Sminthuriformia). It is also suggested that the process is related with the finding of a distorted sex ratio in natural pop ulations and, possibly, with the evolution of parthenogenesis. This hypothe sis is supported by the fact that chromosome pairing and genetic recombinat ion occurs only during female meiosis, while chromosomes do not pair during male meiosis.