Lizards and LINEs: Selection and Demography Affect the Fate of L1 Retrotransposons in the Genome of the Green Anole (Anolis carolinensis)

Tollis, Marc; Boissinot, Stéphane

doi:10.1093/gbe/evt133

Cited by 32 publications

(44 citation statements)

References 65 publications

(138 reference statements)

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“…2012), Anole lizard (Novick et al. 2009; Tollis and Boissinot 2013), Xenopus frogs (Kojima and Fujiwara 2004; Kordis et al. 2006) and African mosquitos (Biedler and Tu 2003).…”

Section: Resultsmentioning

confidence: 99%

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LINEs between Species: Evolutionary Dynamics of LINE-1 Retrotransposons across the Eukaryotic Tree of Life

et al. 2016

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LINE-1 (L1) retrotransposons are dynamic elements. They have the potential to cause great genomic change because of their ability to ‘jump’ around the genome and amplify themselves, resulting in the duplication and rearrangement of regulatory DNA. Active L1, in particular, are often thought of as tightly constrained, homologous and ubiquitous elements with well-characterized domain organization. For the past 30 years, model organisms have been used to define L1s as 6–8 kb sequences containing a 5′-UTR, two open reading frames working harmoniously in cis, and a 3′-UTR with a polyA tail. In this study, we demonstrate the remarkable and overlooked diversity of L1s via a comprehensive phylogenetic analysis of elements from over 500 species from widely divergent branches of the tree of life. The rapid and recent growth of L1 elements in mammalian species is juxtaposed against the diverse lineages found in other metazoans and plants. In fact, some of these previously unexplored mammalian species (e.g. snub-nosed monkey, minke whale) exhibit L1 retrotranspositional ‘hyperactivity’ far surpassing that of human or mouse. In contrast, non-mammalian L1s have become so varied that the current classification system seems to inadequately capture their structural characteristics. Our findings illustrate how both long-term inherited evolutionary patterns and random bursts of activity in individual species can significantly alter genomes, highlighting the importance of L1 dynamics in eukaryotes.

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“…2012), Anole lizard (Novick et al. 2009; Tollis and Boissinot 2013), Xenopus frogs (Kojima and Fujiwara 2004; Kordis et al. 2006) and African mosquitos (Biedler and Tu 2003).…”

Section: Resultsmentioning

confidence: 99%

“…2007; Blass et al. 2012; Tollis and Boissinot 2013; Heitkam et al. 2014) suggests that the current model of L1 activity is insufficient.…”

Section: Introductionmentioning

confidence: 99%

LINEs between Species: Evolutionary Dynamics of LINE-1 Retrotransposons across the Eukaryotic Tree of Life

et al. 2016

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“…In fish and reptiles, very young insertions are over-represented suggesting a low rate of fixation of L1, possibly because novel insertions are under stronger purifying selections in fish and reptiles than they are in mammals (Furano et al 2004; Tollis and Boissinot 2012). This is particularly true for long elements, including full-length ones, which are found at extremely low frequency in natural populations of stickleback (Blass et al 2012) and anole (Tollis and Boissinot 2013), and almost never reach fixation. Consequently, the number of full-length progenitors in a given genome is very small in these species.…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, L1 in non-mammalian vertebrates are represented by much smaller copy numbers, from a few hundreds to several thousand elements, representing <0.5% of their genome size (Hellsten et al 2010; Howe et al 2013). This is likely due to a higher rate of DNA deletion in these genomes but could also reflect variations in the rate of fixation of novel insertions, or both (Duvernell et al 2004; Furano et al 2004; Novick et al 2009; Blass et al 2012; Tollis and Boissinot 2013). …”

Section: Introductionmentioning

confidence: 99%

“…It is thus important to determine the mechanisms responsible for these differences. A number of studies have examined the population dynamics of L1 insertions in mammalian (Boissinot et al 2006; Witherspoon et al 2006; Rishishwar et al 2015) and non-mammalian species (Duvernell, et al 2004; Blass et al 2012; Tollis and Boissinot 2013) but no studies have examined the evolution of the L1 sequence across vertebrates. In fact, almost everything we know about L1, from its structure to its mechanism of transposition, results from studies in mammals, with a focus on human and murine rodents (for a recent review, see Richardson et al 2015).…”

Section: Introductionmentioning

confidence: 99%

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The Evolution of Line-1 in Vertebrates

Boissinot

Sookdeo

2016

Genome Biol Evol

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The abundance and diversity of the LINE-1 (L1) retrotransposon differ greatly among vertebrates. Mammalian genomes contain hundreds of thousands L1s that have accumulated since the origin of mammals. A single group of very similar elements is active at a time in mammals, thus a single lineage of active families has evolved in this group. In contrast, non-mammalian genomes (fish, amphibians, reptiles) harbor a large diversity of concurrently transposing families, which are all represented by very small number of recently inserted copies. Why the pattern of diversity and abundance of L1 is so different among vertebrates remains unknown. To address this issue, we performed a detailed analysis of the evolution of active L1 in 14 mammals and in 3 non-mammalian vertebrate model species. We examined the evolution of base composition and codon bias, the general structure, and the evolution of the different domains of L1 (5′UTR, ORF1, ORF2, 3′UTR). L1s differ substantially in length, base composition, and structure among vertebrates. The most variation is found in the 5′UTR, which is longer in amniotes, and in the ORF1, which tend to evolve faster in mammals. The highly divergent L1 families of lizard, frog, and fish share species-specific features suggesting that they are subjected to the same functional constraints imposed by their host. The relative conservation of the 5′UTR and ORF1 in non-mammalian vertebrates suggests that the repression of transposition by the host does not act in a sequence-specific manner and did not result in an arms race, as is observed in mammals.

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Hybridization and rapid differentiation after secondary contact between the native green anole (Anolis carolinensis) and the introduced green anole (Anolis porcatus)

Wegener

Pita‐Aquino

Atutubo

et al. 2019

Ecology and Evolution

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In allopatric species, reproductive isolation evolves through the accumulation of genetic incompatibilities. The degree of divergence required for complete reproductive isolation is highly variable across taxa, which makes the outcome of secondary contact between allopatric species unpredictable. Since before the Pliocene, two species of Anolis lizards, Anolis carolinensis and Anolis porcatus , have been allopatric, yet this period of independent evolution has not led to substantial species‐specific morphological differentiation, and therefore, they might not be reproductively isolated. In this study, we determined the genetic consequences of localized, secondary contact between the native green anole, A. carolinensis , and the introduced Cuban green anole, A. porcatus , in South Miami. Using 18 microsatellite markers, we found that the South Miami population formed a genetic cluster distinct from both parental species. Mitochondrial DNA revealed maternal A. porcatus ancestry for 35% of the individuals sampled from this population, indicating a high degree of cytonuclear discordance. Thus, hybridization with A. porcatus , not just population structure within A. carolinensis , may be responsible for the genetic distinctiveness of this population. Using tree‐based maximum‐likelihood analysis, we found support for a more recent, secondary introduction of A. porcatus to Florida. Evidence that ~33% of the nuclear DNA resulted from a secondary introduction supports the hybrid origin of the green anole population in South Miami. We used multiple lines of evidence and multiple genetic markers to reconstruct otherwise cryptic patterns of species introduction and hybridization. Genetic evidence for a lack of reproductive isolation, as well as morphological similarities between the two species, supports revising the taxonomy of A. carolinensis to include A. porcatus from western Cuba. Future studies should target the current geographic extent of introgression originating from the past injection of genetic material from Cuban green anoles and determine the consequences for the evolutionary trajectory of green anole populations in southern Florida.

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Lizards and LINEs: Selection and Demography Affect the Fate of L1 Retrotransposons in the Genome of the Green Anole (Anolis carolinensis)

Cited by 32 publications

References 65 publications

LINEs between Species: Evolutionary Dynamics of LINE-1 Retrotransposons across the Eukaryotic Tree of Life

LINEs between Species: Evolutionary Dynamics of LINE-1 Retrotransposons across the Eukaryotic Tree of Life

The Evolution of Line-1 in Vertebrates

Hybridization and rapid differentiation after secondary contact between the native green anole (Anolis carolinensis) and the introduced green anole (Anolis porcatus)

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