CG-rich trinucleotide short tandem repeats (STRs) are linked with human cognition and various neurodevelopmental, neurological, and movement disorders. However, the fundamental two-repeat units of these STRs remain unexplored. On a genome-wide scale, here we mapped the two-repeat units of all combinations of CG-rich trinucleotides in human. We found 81,118 colonies (distance between each unit <500 bp). Subsequently, we performed a comparative genomics study of several large and medium-sized colonies of significant occurrence based on Poisson distribution, in other primates and mouse. We discovered that some of those colonies were shared, with extensive dynamicity, as phylogenetically distant as in mouse. We detected pure units and units that were overlaps of those pure units across the colonies, indicative of unequal crossing over and recombination at those units. We provide example models of some of the potential evolutionary implications of the colonies, such as mechanisms for the emergence and propagation of non-coding RNAs, as well as a defense system against transposable elements, through recombination-coupled inactivating mutations and methylation. In conclusion, we report extensively dynamic trans-species colonies of CG-rich trinucleotide two-repeat units, and indication of crossing over and recombination at those units. Whereas the bulk of literature supports the hypothesis that recombination hotspots rarely (if at all) occur at the same locus between human and chimpanzee, here we propose that sharing such loci may extend beyond primates, and include mouse. Based on the ubiquity, abundance, significant occurrence, and envisioned events and mechanisms associated with the identified colonies, we predict the identified colonies of phenomenal biological and evolutionary consequences.