Symposium: “Evolutionary conflict between mobile DNA and their host genome”

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Michael J. Song and Sarah Schaack (Aug 2018)

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Inner conflict: How mobile DNA wages war and makes peace with host genomes

The Red Queen from Lewis Carroll’s Through the Looking-Glass.
(1871 illustration by John Tenniel)

It is now known that most plant and animal genomes are full of DNA that once could, and in some cases still can, move around. Mobile DNA (also referred to as “selfish” DNA) can either jump from position to position in the genome, or replicate itself and accrue lots of copies over time. In many cases, it will eventually lose ability to move or be silenced by the genome it has invaded. But in some cases, it can be co-opted by the genome it has invaded, and begin to provide important functions for the host instead of simply facilitating its own movement. In this paper, the authors explore the range of possible resolutions to the evolutionary conflict between DNA that can move and replicate and the host genome in which it is found. In order to understand the range of outcomes better, they illustrate the various stages at which conflict can occur and be resolved. Moreover, they highlight the most well-developed bodies of ecological and evolutionary theory from which one can borrow to try and predict the outcomes of conflicts between selfish DNA and their hosts.


Abstract

The proportion of eukaryotic genomes comprised of active or formerly active mobile elements (MEs) is known to vary widely across lineages, but the explanations for why remain largely unknown. Given that ME activity, like other forms of mutation, is thought to be (on average) slightly deleterious in terms of phenotypic effects, understanding the widespread proliferation of MEs in host genomes requires an evolutionary framework. To better develop such a framework, we review the spectrum of resolutions to the genetic conflict between MEs and their hosts: inactivation of MEs due to mutation accumulation, negative selection (or lack thereof) against hosts with high ME loads, silencing of MEs (by hosts or MEs), ME domestication by their hosts, and the horizontal transfer of MEs to new hosts. We also highlight ecological and evolutionary theory from which ME researchers might borrow in order to explain large-scale patterns of ME dynamics across systems. We hope a synthesis of the surprisingly significant role of MEs in the genome, as well as the spectrum of resolutions, applicable theory, and recent discoveries, will have two outcomes for future researchers: better parsing of known variation in ME proliferation patterns across genomes and the development of testable models and predictions regarding the evolutionary trajectory of MEs based on a combination of theory, the comparative method, experimental evolution, and empirical observations.