The influence of transposable elements on animal colouration.

Transposable elements (TEs) are mobile genetic sequences present within host genomes. TEs can contribute to the evolution of host traits, since transposition is mutagenic and TEs often contain host regulatory and protein coding sequences. We review cases where TEs influence animal colouration, reporting major patterns and outstanding questions. TE-induced colouration phenotypes typically arise via introduction of novel regulatory sequences and splice sites, affecting pigment cell development or pigment synthesis. We discuss if particular TE types may be more frequently involved in the evolution of colour variation in animals, given that examples involving long terminal repeat (LTR) elements appear to dominate. Currently, examples of TE-induced colouration phenotypes in animals mainly concern model and domesticated insect and mammal species. However, several influential recent examples, coupled with increases in genome sequencing, suggest cases reported from wild species will increase considerably.

Horizontal transfer and subsequent explosive expansion of a DNA transposon in sea kraits (Laticauda).

Transposable elements (TEs) are self-replicating genetic sequences and are often described as important 'drivers of evolution'. This driving force is because TEs promote genomic novelty by enabling rearrangement, and through exaptation as coding and regulatory elements. However, most TE insertions potentially lead to neutral or harmful outcomes, therefore host genomes have evolved machinery to suppress TE expansion. Through horizontal transposon transfer (HTT) TEs can colonize new genomes, and since new hosts may not be able to regulate subsequent replication, these TEs may proliferate rapidly. Here, we describe HTT of the Harbinger-Snek DNA transposon into sea kraits (Laticauda), and its subsequent explosive expansion within Laticauda genomes. This HTT occurred following the divergence of Laticauda from terrestrial Australian elapids approximately 15-25 Mya. This has resulted in numerous insertions into introns and regulatory regions, with some insertions into exons which appear to have altered UTRs or added sequence to coding exons. Harbinger-Snek has rapidly expanded to make up 8-12% of Laticauda spp. genomes; this is the fastest known expansion of TEs in amniotes following HTT. Genomic changes caused by this rapid expansion may have contributed to adaptation to the amphibious-marine habitat.

Multiple horizontal transfer events of a DNA transposon into turtles, fishes, and a frog.

Horizontal transfer of transposable elements (HTT) has been reported across many species and the impact of such events on genome structure and function has been well described. However, few studies have focused on reptilian genomes, especially HTT events in Testudines (turtles). Here, as a consequence of investigating the repetitive content of Malaclemys terrapin terrapin (Diamondback turtle) we found a high similarity DNA transposon, annotated in RepBase as hAT-6_XT, shared between other turtle species, ray-finned fishes, and a frog. hAT-6_XT was notably absent in reptilian taxa closely related to turtles, such as crocodiles and birds. Successful invasion of DNA transposons into new genomes requires the conservation of specific residues in the encoded transposase, and through structural analysis, these residues were identified indicating some retention of functional transposition activity. We document six recent independent HTT events of a DNA transposon in turtles, which are known to have a low genomic evolutionary rate and ancient repeats.

Detecting Horizontal Transfer of Transposons.

Transposable elements (TEs) are prevalent genomic components which can replicate as a function of mobilization in eukaryotes. Not only do they alter genome structure, they also play regulatory functions or organize chromatin structure. In addition to vertical parent-to-offspring inheritance, TEs can also horizontally "jump" between species, known as horizontal transposon transfer (HTT). This can rapidly alter the course of genome evolution. In this chapter, we provide a practical framework to detect HTT events. Our HTT detection framework is based on the use of sequence alignment to determine the divergence/conservation profiles of TE families to determine the history of expansion events. In summary, it includes (a) workflow of HTT detection from Ab initio identified TEs; (b) workflow for detecting HTT for specific, curated TEs; and (c) workflow for validating detected HTT candidates. Our framework covers two common scenarios of HTT detection in the modern omics era, and we believe it will serve as a valuable toolbox for the TE and genomics research community.

Horizontal Transposon Transfer and Its Implications for the Ancestral Ecology of Hydrophiine Snakes.

Transposable elements (TEs), also known as jumping genes, are sequences able to move or copy themselves within a genome. As TEs move throughout genomes they often act as a source of genetic novelty, hence understanding TE evolution within lineages may help in understanding environmental adaptation. Studies into the TE content of lineages of mammals such as bats have uncovered horizontal transposon transfer (HTT) into these lineages, with squamates often also containing the same TEs. Despite the repeated finding of HTT into squamates, little comparative research has examined the evolution of TEs within squamates. Here we examine a diverse family of Australo-Melanesian snakes (Hydrophiinae) to examine if the previously identified, order-wide pattern of variable TE content and activity holds true on a smaller scale. Hydrophiinae diverged from Asian elapids ~30 Mya and have since rapidly diversified into six amphibious, ~60 marine and ~100 terrestrial species that fill a broad range of ecological niches. We find TE diversity and expansion differs between hydrophiines and their Asian relatives and identify multiple HTTs into Hydrophiinae, including three likely transferred into the ancestral hydrophiine from fish. These HTT events provide the first tangible evidence that Hydrophiinae reached Australia from Asia via a marine route.

Genome Stability Is in the Eye of the Beholder: CR1 Retrotransposon Activity Varies Significantly across Avian Diversity.

Since the sequencing of the zebra finch genome it has become clear that avian genomes, while largely stable in terms of chromosome number and gene synteny, are more dynamic at an intrachromosomal level. A multitude of intrachromosomal rearrangements and significant variation in transposable element (TE) content have been noted across the avian tree. TEs are a source of genome plasticity, because their high similarity enables chromosomal rearrangements through nonallelic homologous recombination, and they have potential for exaptation as regulatory and coding sequences. Previous studies have investigated the activity of the dominant TE in birds, chicken repeat 1 (CR1) retrotransposons, either focusing on their expansion within single orders, or comparing passerines with nonpasserines. Here, we comprehensively investigate and compare the activity of CR1 expansion across orders of birds, finding levels of CR1 activity vary significantly both between and within orders. We describe high levels of TE expansion in genera which have speciated in the last 10 Myr including kiwis, geese, and Amazon parrots; low levels of TE expansion in songbirds across their diversification, and near inactivity of TEs in the cassowary and emu for millions of years. CR1s have remained active over long periods of time across most orders of neognaths, with activity at any one time dominated by one or two families of CR1s. Our findings of higher TE activity in species-rich clades and dominant families of TEs within lineages mirror past findings in mammals and indicate that genome evolution in amniotes relies on universal TE-driven processes.

New Environment, New Invaders-Repeated Horizontal Transfer of LINEs to Sea Snakes.

Although numerous studies have found horizontal transposon transfer (HTT) to be widespread across metazoans, few have focused on HTT in marine ecosystems. To investigate potential recent HTTs into marine species, we searched for novel repetitive elements in sea snakes, a group of elapids which transitioned to a marine habitat at most 18 Ma. Our analysis uncovered repeated HTTs into sea snakes following their marine transition. The seven subfamilies of horizontally transferred LINE retrotransposons we identified in the olive sea snake (Aipysurus laevis) are transcribed, and hence are likely still active and expanding across the genome. A search of 600 metazoan genomes found all seven were absent from other amniotes, including terrestrial elapids, with the most similar LINEs present in fish and marine invertebrates. The one exception was a similar LINE found in sea kraits, a lineage of amphibious elapids which independently transitioned to a marine environment 25 Ma. Our finding of repeated horizontal transfer events into marine snakes greatly expands past findings that the marine environment promotes the transfer of transposons. Transposons are drivers of evolution as sources of genomic sequence and hence genomic novelty. We identified 13 candidate genes for HTT-induced adaptive change based on internal or neighboring HTT LINE insertions. One of these, ADCY4, is of particular interest as a part of the KEGG adaptation pathway "Circadian Entrainment." This provides evidence of the ecological interactions between species influencing evolution of metazoans not only through specific selection pressures, but also by contributing novel genomic material.