In this talk, I will challenge the ‘selfish DNA’ theory and the long-held view that active transposons are merely in conflict with their host. I will argue for a more nuanced view in which transposons and their host engage in mutualistic activities. Mutualistic interactions are well established for bacterial mobile elements, but scarcely documented for eukaryotic transposons. We postulate that give-and-take interactions between eukaryotic transposons and their hosts are more common than currently recognized and arise progressively during evolution as an addiction to transposon-encoded products. We hypothesize that some transposons encode products with cellular activities that encroach on and occasionally replace host functional processes during development in a way that create a dependency on transposon products for host development. These dose-dependent interactions would promote the maintenance of the transposon in the germline but establish a form of copy number control mechanism that would benefit both the host and transposons. This model, which we call ‘transposon addiction’ makes predictions that we are testing using zebrafish and chicken. We focus on several endogenous retroviruses that are likely transpositionally active in these species and have evolved precise developmental expression in somatic cell lineages where we predict ‘addictive’ interactions to develop. Manipulative experiments show that the Gag proteins encoded by three different endogenous retrovirus families in zebrafish and chick embryos are required for mesoderm development and neural crest migration respectively. Our data support the provocative idea that transposon activities are inextricably intertwined with organismal development, as envisioned by Barbara McClintock but largely dismissed for more than half a century.