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

Linquist, Stefan; Cottenie, Karl; Elliott, Tyler A.; Saylor, Brent; Kremer, Stefan C.; Gregory, T. Ryan

doi:10.1111/mec.13219

Cited by 38 publications

(34 citation statements)

References 56 publications

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“…It has been recently suggested that the relationships between genome components (including genes, transposable elements, or any sequence able to persist over evolutionary time) were similar to the relationships between individuals or species in ecosystems (10,49,50), although the possibility to apply ecological formalism to genome evolution remains questionable (51). Here, we brought substantial evidence that the relationships between autonomous and nonautonomous mariner TE copies were analogous to parasitism: Mos1 copies (the "hosts") are able to survive and replicate by themselves, whereas peach copies (the "parasites") are unable to transpose without Mos1 copies.…”

Section: Discussionmentioning

confidence: 99%

Experimental evolution reveals hyperparasitic interactions among transposable elements

Robillard

Rouzic

Zhang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Transposable elements (TEs) are repeated DNA sequences that can constitute a substantial part of genomes. Studying TEs' activity, interactions, and accumulation dynamics is thus of major interest to understand genome evolution. Here, we describe the transposition dynamics of cut-and-paste mariner elements during experimental (short-and longer-term) evolution in Drosophila melanogaster. Flies with autonomous and nonautonomous mariner copies were introduced in populations containing no active mariner, and TE accumulation was tracked by quantitative PCR for up to 100 generations. Our results demonstrate that (i) active mariner elements are highly invasive and characterized by an elevated transposition rate, confirming their capacity to spread in populations, as predicted by the "selfish-DNA" mechanism; (ii) nonautonomous copies act as parasites of autonomous mariner elements by hijacking the transposition machinery produced by active mariner, which can be considered as a case of hyperparasitism; (iii) this behavior resulted in a failure of active copies to amplify which systematically drove the whole family to extinction in less than 100 generations. This study nicely illustrates how the presence of transposition-competitive variants can deeply impair TE dynamics and gives clues to the extraordinary diversity of TE evolutionary histories observed in genomes.transposable elements | hyperparasitism | Drosophila | experimental evolution | invasion dynamics

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Section: Discussionmentioning

confidence: 99%

Experimental evolution reveals hyperparasitic interactions among transposable elements

Robillard

Rouzic

Zhang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…As a result of this conflict, many genomes are littered with a bulk of TE-derived DNA that is often relatively transcriptionally and recombinationally inert (Fedoroff, 2012). But while this conflict between TEs and their host has long been noted to shape general patterns of TE evolution (Charlesworth and Charlesworth, 1983;Charlesworth and Langley, 1989;Kidwell and Lisch, 1997;Venner et al, 2009), the details of how this conflict unfolds are tenuous and rarely well understood (Linquist et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

The Genomic Ecosystem of Transposable Elements in Maize

Stitzer¹,

Anderson

Springer

et al. 2019

Preprint

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Transposable elements (TEs) constitute the majority of flowering plant DNA, reflecting their tremendous success in subverting, avoiding, and surviving the defenses of their host genomes to ensure their selfish replication. More than 85% of the sequence of the maize genome can be ascribed to past transposition, providing a major contribution to the structure of the genome. Evidence from individual loci has informed our understanding of how transposition has shaped the genome, and a number of individual TE insertions have been causally linked to dramatic phenotypic changes. But genome-wide analyses in maize and other taxa have frequently represented TEs as a relatively homogeneous class of fragmentary relics of past transposition, obscuring their evolutionary history and interaction with their host genome. Using an updated annotation of structurally intact TEs in the maize reference genome, we investigate the family-level ecological and evolutionary dynamics of TEs in maize. Integrating a variety of data, from descriptors of individual TEs like coding capacity, expression, and methylation, as well as similar features of the sequence they inserted into, we model the relationship between these attributes of the genomic environment and the survival of TE copies and families. Our analyses reveal a diversity of ecological strategies of TE families, each representing the evolution of a distinct ecological niche allowing survival of the TE family. In contrast to the wholesale relegation of all TEs to a single category of junk DNA, these differences generate a rich ecology of the genome, suggesting families of TEs that coexist in time and space compete and cooperate with each other. We conclude that while the impact of transposition is highly family-and context-dependent, a family-level understanding of the ecology of TEs in the genome can refine our ability to predict the role of TEs in generating genetic and phenotypic diversity. transposable elements | ecology | maize Correspondence: mcstitzer@ucdavis.edu 'Lumping our beautiful collection of transposons into a single category is a crime' -Michael R. Freeling,

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“…genome size evolution | DNA loss | transposable elements | amniotes | flight T he nature and relative importance of the molecular mechanisms and evolutionary forces underlying genome size variation has been the subject of intense research and debate (1)(2)(3)(4)(5)(6)(7). Variation in genome sizes may not always occur at a level where natural selection is strong enough to prevent genetic drift to determine their fate (neutral or effectively neutral variation) (3).…”

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confidence: 99%

Dynamics of genome size evolution in birds and mammals

Kapusta

Suh

Feschotte

2017

Proc. Natl. Acad. Sci. U.S.A.

369

358

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Genome size in mammals and birds shows remarkably little interspecific variation compared with other taxa. However, genome sequencing has revealed that many mammal and bird lineages have experienced differential rates of transposable element (TE) accumulation, which would be predicted to cause substantial variation in genome size between species. Thus, we hypothesize that there has been covariation between the amount of DNA gained by transposition and lost by deletion during mammal and avian evolution, resulting in genome size equilibrium. To test this model, we develop computational methods to quantify the amount of DNA gained by TE expansion and lost by deletion over the last 100 My in the lineages of 10 species of eutherian mammals and 24 species of birds. The results reveal extensive variation in the amount of DNA gained via lineage-specific transposition, but that DNA loss counteracted this expansion to various extents across lineages. Our analysis of the rate and size spectrum of deletion events implies that DNA removal in both mammals and birds has proceeded mostly through large segmental deletions (>10 kb). These findings support a unified "accordion" model of genome size evolution in eukaryotes whereby DNA loss counteracting TE expansion is a major determinant of genome size. Furthermore, we propose that extensive DNA loss, and not necessarily a dearth of TE activity, has been the primary force maintaining the greater genomic compaction of flying birds and bats relative to their flightless relatives.genome size evolution | DNA loss | transposable elements | amniotes | flight T he nature and relative importance of the molecular mechanisms and evolutionary forces underlying genome size variation has been the subject of intense research and debate (1-7). Variation in genome sizes may not always occur at a level where natural selection is strong enough to prevent genetic drift to determine their fate (neutral or effectively neutral variation) (3). Additionally, the fixation probability of slightly deleterious deletions or insertions would be higher in species with smaller effective population sizes, where natural selection acts less efficiently (3,8). On the other hand, a number of correlative associations between genome size and phenotypic traits, such as cell size (9, 10) and metabolic rate associated with powered flight (11, 12), suggest that natural selection and adaptive processes also shape genome size evolution. Teasing apart the relative importance of these two forces (drift and selection) requires a better understanding of the mode and processes by which DNA is gained and lost over long evolutionary periods in different taxa. Thus, establishing an integrated view of the contribution of gain and loss of DNA to genome size variation (or lack thereof) remains an important goal in genome biology (e.g., refs. 1, 2, 13, and 14).Most studies of genome size evolution have focused on taxa with extensive variation in genome sizes, such as flowering plants (15)(16)(17)(18)(19)(20), conifers (21), insects (22-...

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

Cited by 38 publications

References 56 publications

Experimental evolution reveals hyperparasitic interactions among transposable elements

Experimental evolution reveals hyperparasitic interactions among transposable elements

The Genomic Ecosystem of Transposable Elements in Maize

Dynamics of genome size evolution in birds and mammals

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