Profuse evolutionary diversification and speciation on volcanic islands: transposon instability and amplification bursts explain the genetic paradox

Elysse M. Craddock

Species-rich adaptive radiations arising from rare plant and animal colonizers are common on remote volcanic archipelagoes. However, they present a paradox. The severe genetic bottleneck of founder events and effects of inbreeding depression, coupled with the inherently stressful volcanic environment, would seem to predict reduced evolutionary potential and increased risk of extinction, rather than rapid adaptive divergence and speciation. Significantly, eukaryotic genomes harbor many families of transposable elements (TEs) that are mobilized by genome shock; these elements may be the primary drivers of genetic reorganization and speciation on volcanic islands. Here I propose that a central factor in the spectacular radiation and diversification of the endemic Hawaiian Drosophila and other terrestrial lineages on the Hawaiian and other oceanic islands has been repeated bursts of transposition of multiple TEs induced by the unique ecological features of volcanic habitats. Founder individuals and populations on remote volcanic islands experience significant levels of physiological and genomic stress as a consequence of both biotic and abiotic factors. This results in disruption of the usual epigenetic suppression of TEs, unleashing them to proliferate and spread, which in turn gives rise to novel genetic variation and remodels genomic regulatory circuits, facilitating rapid morphological, ecological and behavioral change, and adaptive radiation. To obtain empirical support for the hypothesis, test organisms should be exposed to prolonged heat stress, high levels of carbon dioxide and other volcanic gases, along with inbreeding. Data from subsequent whole genome sequencing and bioinformatics screening for TE numbers and locations would then be compared with initial pre-exposure TE information for the test strains, a labor-intensive project. Several predicted outcomes arising from the hypothesis are discussed. Currently available data are consistent with the proposed concept of stress-induced TE mobilization as a trigger of evolutionary diversification and speciation on volcanic islands. The main implication is that both TEs and species should proliferate at a much higher rate on volcanic islands than elsewhere. Second, the evolvability of a lineage may correlate with the abundance and distribution of TEs in the genome. Successful colonizers of volcanic habitats with high genomic proportions of TEs may be best poised to found a speciose lineage that gives rise to a dramatic adaptive radiation. Colonizers that are depauperate in TEs are likely to be evolutionarily constrained and diversify little, if at all. This article was reviewed by Dr. James Shapiro and Dr. Wolfgang Miller (nominated by Editorial Board member Dr. I. King Jordan).