Meiotic Models to Explain Classical Linkage, Pseudolinkage, and Chromosomal Pairing in Tetraploid Derivative Salmonid Genomes: II. Wright is Still Right

The purpose of the article by Allendorf et al. (2015) in the words of the authors is “(1) to synthesize what is known about the transmission genetics of salmonid fishes and (2) to consider how ignoring these patterns could lead to erroneous conclusions about their genomic organization and population genetics.” The first section of the article is designed to bring the reader up to speed on what is currently known about transmission genetics in salmonid fishes. The glossary of terms is an important addition to this effort. Allendorf et al. (2015), explain very well the issues surrounding the practice and significance of ignoring loci in the telomeric regions of homeologous arms and this section will be of interest to all geneticists who work on polyploid and polyploid derivative organisms. However, the chromosomal pairing models presented are misleading, as they do not incorporate the available chromosomal evidence. Further their explanations of how their models differ from Wright et al. (1983) are unsupported and confusing given the models presented. Herein we elaborate on the chromosomal pairing models of Wright et al. (1983) based on cytogenetic evidence to improve understanding of the intriguing complex chromosomal pairing and segregation patterns observed in salmonid male meioses. The chromosomal pattern for residual tetrasomy (Figure 1; Allendorf et al. 2015) derives from earlier work, starting with an original proposal by Allendorf and Thorgaard (1984, see Figure 4 therein). In the 1984 article, they showed a model of 4 acrocentrics in a multivalent pairing configuration. The original model had only one crossover between 2 of the homeologous arms of the acrocentrics. They proposed this as a general model with no specificity regarding chromosomal behavior. An update by Allendorf and Danzmann (1997) added 2 crossovers in the disomic regions of the homologous chromosome arms close to centromeres, keeping the acrocentric model and assuming 3 crossover events among these 4 arms. This was also proposed to be a general model, but in fact is even more complex and ignored the available chromosomal evidence (Davisson et al. 1973; Lee and Wright 1981). Allendorf and Danzmann (1997) state “we have no direct chromosomal evidence for this model in salmonids”. In Figure 1 of Allendorf et al. (2015), a set of metacentric chromosomes replaces one of the sets of acrocentrics and one of the crossovers is moved from one side of the centromere to the opposite arm of the newly added metacentric. The essence of this model is that at first the homologous chromosomes pair completely and then the homeologous arms pair, introducing an additional crossover event in one of the arms already involved in a crossover. While the authors cite evidence from other organisms for secondary pairing of chromosomes already paired, it is not the most parsimonious explanation for residual tetrasomy in salmonids. The caveat proposed in support of their model in the authors’ words is “Figure 1 shows one of several possible chiasmata formations where this model would support equational division.”, but this caveat does not lend any more support for this model. What are some of these other possible chiasmata, other than that proposed by the Wright model? It is unclear how this configuration could unfold and give the long multivalent rods observed during Meiosis I. In Figure 3, Allendorf et al. (2015) have drawn up a new model to explain pseudolinkage. Surprisingly, their model for pseudolinkage, unlike in Figure 1 for residual tetrasomy, does not involve 4 chromosome arms pairing and multiple crossovers in the same arm. This proposal would suggest that residual tetrasomy and pseudolinkage are 2 different phenomena and not that pseudolinkage is a specialized case of residual tetrasomy. It is interesting that they show 2 metacentrics and 2 accrocentrics for residual tetrasomy and 4 metacentrics for pseudolinkage. Further, Figure 3, although technically correct in pairing and crossover events, is displayed in a fashion making it largely impossible to understand chromosomal segregation. Note the extra-large crossover event and the inversion of the grey arms into proximity with the black arms that are clearly neither homologous nor homeologous. In the late 1970s and early 1980s the late Dr James E. Wright, Jr., who had been studying salmonid meiotic chromosome pairing in males and females simultaneously with allozyme segregation patterns for over 10 years, assembled a team of graduate students and technicians who worked together on the unusual patterns of “multivalent” pairing in male meioses and allozyme segregation patterns. These 2 lines of research and the resultant data were integrated to Journal of Heredity Advance Access published August 29, 2015