Distinguishing ecological from evolutionary approaches to transposable elements

Abstract

Considerable variation exists not only in the kinds of transposable elements (TEs) occurring within the genomes of different species, but also in their abundance and distribution. Noting a similarity to the assortment of organisms among ecosystems, some researchers have called for an ecological approach to the study of transposon dynamics. However, there are several ways to adopt such an approach, and it is sometimes unclear what an ecological perspective will add to the existing co-evolutionary framework for explaining transposon-host interactions. This review aims to clarify the conceptual foundations of transposon ecology in order to evaluate its explanatory prospects. We begin by identifying three unanswered questions regarding the abundance and distribution of TEs that potentially call for an ecological explanation. We then offer an operational distinction between evolutionary and ecological approaches to these questions. By determining the amount of variance in transposon abundance and distribution that is explained by ecological and evolutionary factors, respectively, it is possible empirically to assess the prospects for each of these explanatory frameworks. To illustrate how this methodology applies to a concrete example, we analyzed whole-genome data for one set of distantly related mammals and another more closely related group of arthropods. Our expectation was that ecological factors are most informative for explaining differences among individual TE lineages, rather than TE families, and for explaining their distribution among closely related as opposed to distantly related host genomes. We found that, in these data sets, ecological factors do in fact explain most of the variation in TE abundance and distribution among TE lineages across less distantly related host organisms. Evolutionary factors were not significant at these levels. However, the explanatory roles of evolution and ecology become inverted at the level of TE families or among more distantly related genomes. Not only does this example demonstrate the utility of our distinction between ecological and evolutionary perspectives, it further suggests an appropriate explanatory domain for the burgeoning discipline of transposon ecology. The fact that ecological processes appear to be impacting TE lineages over relatively short time scales further raises the possibility that transposons might serve as useful model systems for testing more general hypotheses in ecology.

Against Lawton’s Contingency Thesis; or, Why the Reported Demise of Community Ecology Is Greatly Exaggerated

“…For that matter, what makes a generalization ecological in the first place? A candidate solution to these questions has recently emerged within the field of genome ecology (Linquist et al 2013). This burgeoning subdiscipline applies ecological thinking at the level of the genome, viewing families of mobile genetic elements as akin to species and stable features of the genome as the environment (Brookfield, 2005).…”

“…There is no need to adopt a more complicated hybrid model if a simpler model will do. Within genome ecology a straightforward strategy has been developed to determine the extent to which a given pattern can be explained by ecological or evolutionary factors (Linquist et al 2013). One begins with a dependent variable of interest.…”

“…Specifically, it views these two types of explanation as mutually exclusive. An alternative picture has recently been developed in the field of genome ecology (Linquist et al 2013), which can be applied to the community level.…”

Molecules and Macroevolution: A Gouldian View of the Genome

“…Some TEs may be reliant on others for their survival, as with the dependency of SINEs on LINEs for propagation. The list of ecological parallels could go on, and shows that there is much more to evolution within the genome than simple antagonism between TEs and their hosts (Linquist et al 2013). Of course, this is only one level of interest among several.…”

Applying ecological models to communities of genetic elements: the case of neutral theory

“…; Linquist et al . ). The central idea is that genomes can be viewed as ecosystems in miniature, where particular DNA sequences are compared to organisms and the surrounding genetic and cellular structures are regarded as the local environment.…”