Serendipitous adaptive evolutionary innovation mediated by methylome and TE mobilome dynamics

How is it that invasive species can rapidly adapt and diversify when they colonise a novel or challenging environment? Theory predicts that those few founding individuals that colonise a new location will have reduced levels of genetic diversity, placing them at a selective and evolutionary disadvantage. Clearly, the traditional paradigm that adaptive potential of introduced species is governed by levels of standing genetic diversity defined by the slow accumulation of DNA mutations needs to be revised.

We need to identify novel mechanisms through which genetic innovation can be generated that allows for rapid adaptation. Such new insight would provide novel understanding of evolution and has implications for how we manage some major societal challenges, including the appearance and spread of crop pests and non-native alien invasives, the emergence of zoonotic disease and the resilience of species to environmental perturbation.

Here we examine the role that transposable elements (TE), pieces of parasitic DNA that copy themselves and move about through a host's genome, can play in generating spontaneous and serendipitous genetic innovations for their host, so facilitating adaptive potential. TE can have a range of effects on host genes, impacting gene expression if they land around promotor regions, or altering genome architecture by gene duplication or ectopic recombination.

Crucially, TE are responsive to environmental change, being activated by environmental stress and allowed to proliferate by the disruption of mechanisms hosts use to suppress TE activity, especially methylation of CG nucleotide motifs. So, the capacity for an organism to rapidly adapt to a new environment may be driven by the act of colonisation itself, with environmentally induced stress increasing TE activity that then generates novel beneficial mutations that facilitate adaptation.

Examining this potential role of TE in driving adaptive potential has hitherto been impossible because of an inability to characterise TE diversity, abundance and location in relation to host genes (the host "mobilome"), and simultaneously determine how TE are being policed by methylation (the TE "methylome"). Recent advances in Nanopore DNA sequencing yield long DNA sequence reads that can both identify TE and anchor their locations in a host genome, plus simultaneously determine the methylation status of TE.

Moreover, this can be done from low-coverage genome skims that provides unprecedented comparative analysis across species to ascertain how evolutionary innovation is generated through different, parallel or convergent routes across different species invading the same environment.