No genome is an island: toward a 21st century agenda for evolution

Conventional 20th century evolution thinking was based on the idea of isolated genomes for each species. Any possibility of life-history inputs to the germ line was strictly excluded by Weismann's doctrine, and genome change was attributed to random copying errors. Today, we know that many life-history events lead to rapid and nonrandom evolutionary change mediated by specific cellular functions. There are many ways that genomes, viruses, cells, and organisms interact to generate evolutionary variation. These include cell mergers and activation of natural genetic engineering by stress, infection, and interspecific hybridization. In addition, we know molecular mechanisms for transmitting life-history information across generations through gametes. These discoveries require a new agenda for evolutionary theory and novel experimental designs to investigate the genomic impacts of stresses, biotic interactions, and sensory inputs coming from the environment. The review will offer some generic recommendations for enriching evolution experiments to incorporate new knowledge and find answers to previously excluded questions.