SYNAPTIC ADAPTATION IN DEER MICE: A CELLULAR MECHANISM FOR KARYOTYPIC ORTHOSELECTION

While the kinds of karyotypic differences between closely related species vary greatly from group to group, chromosomal evolution within particular lineages often involves the establishment of similar structural changes in one karyotype after another. This pattern of chromosomal evolution, termed karyotypic orthoselection (White, 1973, 1975), is known to include a diversity of types of structural changes in a variety of groups of organisms. The underlying cellular bases of karyotypic orthoselection, however, remain unknown. White (1975, 1978) suggested four possible explanations for karyotypic orthoselection: differential origin (of mutation types), external adaptation (differential selection), cytomechanical restraints (imposing limits on the number of chromosomes or chromosomal arms), and architectural regularity of the chromosomes themselves and/or their spatial associations in interphase nuclei. Of these, only regularity of the intranuclear architecture was considered likely to explain karyotypic orthoselection (White, 1975, 1978). Recent studies documenting nonrandom orientations of chromosomes in interphase nuclei (Bennett, 1982; Agard and Sedat, 1983; Mathog et al., 1984) suggest that architectural regularities may play a central role in the ways in which chromosomes evolve. Research in this area, however, has yet to document a widely applicable mechanism such as would be necessary to regulate the various expressions of karyotypic orthoselection. Chromosomal evolution involving euchromatic rearrangements is generally considered to involve the fixation of arrangements which substantially reduce the fertility of heterozygotes. If certain rearrangements can be shown to be less susceptible to the production of genetically unbalanced gametes within particular evolutionary lineages, however, then these rearrangements might be expected to become fixed in a pattern of karyotypic orthoselection. In this report, we present data which suggest that synapsis in deer mice, Peromyscus, is characteristically different for two types of spontaneously occurring chromosomal rearrangements, with the orthoselected type of rearrangement apparently resulting in no loss of heterozygote fitness. We hypothesize that such synaptic adaptation may function as a primary factor in the generation of karyotypic orthoselection. All species of Peromyscus for which karyotypic data are available have a diploid number of 48. Variation in the number of arms in the autosomal complement is extensive, however, ranging from 52 to 92. G-banding studies, including 30 species of Peromyscus (Rogers et al., 1984; Stangi and Baker, 1984), indicate that no fewer than 38 separate pericentric inversions have been incorporated during the chromosomal evolution of this genus. Additionally, several species exhibit intraspecific polymorphisms for pericentric inversions (Greenbaum et al., 1978; Baker et al., 1983; Pengilly et al., 1983; Greenbaum and Reed, 1984). Most of the inversions that occur within and among species of Peromyscus are of lengths which should substantially reduce the reproductive fitness of heterozygotes. Except for differences in the presence or absence of heterochromatic segments, no other types of chromosomal rearrangements have been documented in deer mice as either spontaneous events within individuals or as evolutionary events among populations or species. In a light-microscopic study of synaptonemal complex (SC) from P. maniculatus heterozygous for a terminally positioned pericentric inversion of chromosome 6, Greenbaum and Reed (1984) reported regularly formed autosomal pairs in the majority of cells examined; inversion loops were observed at a frequency of less than 1%. It was hypothesized that heterosynapsis of the inverted segment blocks crossing over, eliminates the production of duplication and deletion chromatids, and thus provides an evolutionary mechanism which facilitates the incorporation of pericentric inversions. During electron microscopic studies of SC in Peromyscus, we have obtained data which corroborate the findings of Greenbaum and Reed (1984) and document homologous pairing for three spontaneous rearrangements interpreted as translocations in the primary spermatocytes. Whole cell complements of surface spread SCs were prepared by the method of Counce and Meyer (1973), as modified for mammalian testicular material by Moses (1977), and stained with silver nitrate using the method of Howell and Black (1980). A total of seven Peromyscus (four P. maniculatus and three P. sitkensis) were examined with SCs analyzed for more than 520 zygotene and pachytene nuclei. A detailed analysis of the mechanisms of meiotic pairing based on six of these specimens (excluding the individual of P. sitkensis reported below) is presented by Greenbaum et al. (1986). The somatic karyotype of each specimen was characterized from standard and Gand C-banded mi-