Long-term TE persistence even without beneficial insertion.

This correspondence responds to the critique by Butler et al. (BMC Genomics 22:241, 2021) of our recent paper on transposable element (TE) persistence. We address the three main objections raised by Butler et al. After running a series of additional simulations that were inspired by the authors' criticisms, we are able to present a more nuanced understanding of the conditions that generate long-term persistence.

Transposable element persistence via potential genome-level ecosystem engineering.

BACKGROUND: The nuclear genomes of eukaryotes vary enormously in size, with much of this variability attributable to differential accumulation of transposable elements (TEs). To date, the precise evolutionary and ecological conditions influencing TE accumulation remain poorly understood. Most previous attempts to identify these conditions have focused on evolutionary processes occurring at the host organism level, whereas we explore a TE ecology explanation. RESULTS: As an alternative (or additional) hypothesis, we propose that ecological mechanisms occurring within the host cell may contribute to patterns of TE accumulation. To test this idea, we conducted a series of experiments using a simulated asexual TE/host system. Each experiment tracked the accumulation rate for a given type of TE within a particular host genome. TEs in this system had a net deleterious effect on host fitness, which did not change over the course of experiments. As one might expect, in the majority of experiments TEs were either purged from the genome or drove the host population to extinction. However, in an intriguing handful of cases, TEs co-existed with hosts and accumulated to very large numbers. This tended to occur when TEs achieved a stable density relative to non-TE sequences in the genome (as opposed to reaching any particular absolute number). In our model, the only way to maintain a stable density was for TEs to generate new, inactive copies at a rate that balanced with the production of active (replicating) copies. CONCLUSIONS: From a TE ecology perspective, we suggest this could be interpreted as a case of ecosystem engineering within the genome, where TEs persist by creating their own "habitat".

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

A promising recent development in molecular biology involves viewing the genome as a mini-ecosystem, where genetic elements are compared to organisms and the surrounding cellular and genomic structures are regarded as the local environment. Here, we critically evaluate the prospects of ecological neutral theory (ENT), a popular model in ecology, as it applies at the genomic level. This assessment requires an overview of the controversy surrounding neutral models in community ecology. In particular, we discuss the limitations of using ENT both as an explanation of community dynamics and as a null hypothesis. We then analyse a case study in which ENT has been applied to genomic data. Our central finding is that genetic elements do not conform to the requirements of ENT once its assumptions and limitations are made explicit. We further compare this genome-level application of ENT to two other, more familiar approaches in genomics that rely on neutral mechanisms: Kimura's molecular neutral theory and Lynch's mutational-hazard model. Interestingly, this comparison reveals that there are two distinct concepts of neutrality associated with these models, which we dub 'fitness neutrality' and 'competitive neutrality'. This distinction helps to clarify the various roles for neutral models in genomics, for example in explaining the evolution of genome size.

A novel application of ecological analyses to assess transposable element distributions in the genome of the domestic cow, Bos taurus.

Transposable elements (TEs) are among the most abundant components of many eukaryotic genomes. Efforts to explain TE abundance, as well as TE diversity among genomes, have led some researchers to draw an analogy between genomic and ecological processes. Adopting this perspective, we conducted an analysis of the cow (Bos taurus) genome using techniques developed by community ecologists to determine whether environmental factors influence community composition. Specifically, each chromosome within the Bos taurus genome was treated as a "linear transect", and a multivariate redundancy analysis (RDA) was used to identify large-scale spatial patterns in TE communities associated with 10 TE families. The position of each TE community on the chromosome accounted for ∼50% of the variation along the chromosome "transect". Multivariate analysis further revealed an effect of gene density on TE communities that is influenced by several other factors in the (genomic) environment, including chromosome length and TE density. The results of this analysis demonstrate that ecological methods can be applied successfully to help answer genomic questions.

Yes! There are resilient generalizations (or "laws") in ecology.

ABSTRACT It is often argued that ecological communities admit of no useful generalizations or "laws" because these systems are especially prone to contingent historical events. Detractors respond that this argument assumes an overly stringent definition of laws of nature. Under a more relaxed conception, it is argued that ecological laws emerge at the level of communities and elsewhere. A brief review of this debate reveals an issue with deep philosophical roots that is unlikely to be resolved by a better understanding of generalizations in ecology. We therefore propose a strategy for transforming the conceptual question about the nature of ecological laws into a set of empirically tractable hypotheses about the relative re- silience of ecological generalizations across three dimensions: taxonomy, habitat type, and scale. These hypotheses are tested using a survey of 240 meta-analyses in ecology. Our central finding is that generalizations in community ecology are just as prevalent and as resilient as those in population or ecosystem ecology. These findings should help to establish community ecology as a generality-seeking science as opposed to a science of case studies. It also supports the capacity for ecologists, working at any of the three levels, to inform matters of public policy.

Distinguishing ecological from evolutionary approaches to transposable elements.

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.