Estimation of the Highest Chromosome Number of Eukaryotes Based on the Minimum Interaction Theory

Abstract

According to the minimum interaction theory, the chromosome evolution of eukaryotes proceeds as a whole toward increasing the chromosome number. This raises the following two questions: what was the starting chromosome number of eukaryotes and does the chromosome number increase infinitely? We attempted to provide a theoretical framework to resolve these questions. We propose that the species with n=2 observed in Protozoa, Platyhelminthes, Annelid, Algae, Fungi and higher plants would be chromosomal relicts conserving the karyotypes of ancestral eukaryotes. We also propose that the ideal highest number of eukaryotes ( n max ) can be given by an inverse of the minimum terminal interference distance ( It min ) in crossing-over ( n max =100/ It min ). As It min =0.6 in mammals, n max ≈166. On the other hand, the value estimated by computer simulations is somewhat lower with n max =133–138. Our arguments can be applied to other eukaryotes, if they have a localized centromere and the ratio of total synaptonemal complex/nuclear volume is comparable to that of mammals. We revealed that the index of gene shuffling per karyotypes ( G) by means of the total number of gamete types with different gene combinations can be formulated as G =2 n+ Fxi , where Fxi means interstitial chiasma frequency per cell corresponding to crossing-over mediated by the recombination nodule. The Fxi value increases in proportion to the n value in areas where n<40, but decreases gradually when n>40 and becomes zero when n>83. Therefore, in the ultimate karyotype with n max =166, FXi=0 and G =2 n =2 166, where gene shuffling is guaranteed by the random orientation of chromosomes at the equatorial plate of meiotic metaphase I.