Mobile DNA and evolution in the 21st century

Abstract: Scientific history has a profound effect on theories of evolution. At the beginning of the 21 st Century, molecular cell biology has revealed a dense structure of information-processing networks that use the genome as an interactive Read-Write (RW) memory system rather than an organism blueprint. Genome sequencing has documented the importance of mobile DNA activities and major genome restructuring events at key junctures in evolution: exon shuffling, changes in cis-regulatory sites, horizontal transfer, cell fusions, and whole genome doublings (WGDs). The natural genetic engineering functions that mediate genome restructuring are activated by multiple stimuli, in particular by events similar to those found in the DNA record: microbial infection and interspecific hybridization leading to the formation of allotetraploids. These molecular genetic discoveries, plus a consideration of how mobile DNA rearrangements increase the efficiency of generating functional genomic novelties, make it possible to formulate a 21 st Century view of interactive evolutionary processes. This view integrates contemporary knowledge of the molecular basis of genetic change, major genome events in evolution, and stimuli that activate DNA restructuring with classical cytogenetic understanding about the role of hybridization in species diversification. Shapiro Page 2 Evolution in the 21st Century Introduction: Summary of the argument The review assumes that readers of this journal are familiar with the actions of mobile DNA and other genome restructuring functions. It will try to integrate that familiarity into the historical development of evolutionary concepts and incorporate recent discoveries from genome sequencing. Just as our knowledge of mobile DNA has introduced new ways of thinking about hereditary change, the results of sequence analysis have documented several types of genome alterations at key places in evolutionary history which happened within a single generation and affected multiple cellular and organismal characters at the same time: horizontal transfer of large DNA segments, cell fusions and symbioses, and whole genome doublings (WGDs). These rapid multi-character changes are fundamentally different from the slowly accumulating small random variations postulated in Darwinian and neo-Darwinian theory. Cell mergers and WGDs are the kinds of events that activate mobile DNA and genome restructuring. In order to fully integrate the genomic findings with our knowledge of mobile DNA, we have to make use of information about the molecular regulation of mobile DNA activities as well as McClintock's view that cells respond to signs of danger, frequently restructuring their genomes as part of the respons