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

Abstract

While 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 Mya. Our analysis uncovered repeated HTTs into sea snakes following their marine transition. The 7 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 7 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 Mya. Our finding of repeated horizontal transfer events into marine snakes greatly expands past findingst 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 neighbouring 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.

Impact of Repetitive DNA Elements on Snake Genome Biology and Evolution

“…All six primitive snake species compared ( Figure 2 ) were found to display a low abundance of CR1 and LTRs, which were higher than those in many species ( Deinagkistrodon acutus , Bothrops asper , Cerrophidion godmani , Sistrurus catenatus , Crotalus atrox , C. viridis ) of the advanced snake lineage. In addition, BovB is found at high abundance in the genome of the marine file snake ( Figure 2 ) ( Acrochordus granulatus ), which is indicative of HTT events as also reported by Galbraith et al [ 48 ] in several species of sea snake. This variability can contribute to genome diversification between primitive and advanced snakes, and even to variation in species-specific elements, thereby reshaping homomorphic or heterophonic sex chromosomes and karyotypic variability with different numbers of microchromosomes.…”

“…For example, the transcriptional activity of LINEs in amphibious elapids provides evidence that these elements may drive ecological adaptation in marine environments. Interestingly, active LINEs are exclusively present in sea snakes and are localized in the vicinity of “ADCY4”, a gene involved in circadian entrainment [ 48 ]. Several other genes involved in the functions of adaptive features (metabolism, development, limb loss, trunk elongation, and skeletal changes) have been detected with rapid and extremely variable transcriptional responses in multiple organ systems under different environments [ 12 , 13 , 22 , 226 ].…”

“…Due to their phenotypically diverse radiation, snakes have become increasingly important model systems for developmental biology, evolutionary ecology, and molecular evolution and adaptation. Snakes appear prone to the horizontal transfer of TEs (HTT) and microsatellite seeding [ 40 , 47 , 48 ]. In addition, snakes exhibit unique characteristics related to sex determination systems.…”

The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

“…CR1) and LTR retrotransposons (ERVs). For DNA transposons and LINEs, we first identified open reading frames (ORFs) in the insertions annotated by R epeat M asker , then translated such ORFs and aligned with RPS-BLAST [ 102 ] against a custom Pfam [ 103 ] database containing transposon-related proteins (similar approach to [ 104 ]). ORFs from LINEs of at least 600 bp that spanned 90% of both endonuclease and reverse transcriptase domains were considered as full-length elements.…”

The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

“…We identified fl-TEs in all the six avian genomes by adopting different methods for DNA transposons, LINEs (e.g., CR1), and LTR retrotransposons (ERVs). For DNA transposons and LINEs, we first identified open reading frames (ORFs) in the insertions annotated by RepeatMasker, then translated such ORFs and aligned with RPS-BLAST [103] against a custom Pfam [104] database containing transposon-related proteins (similar approach to [105]). ORFs from LINEs of at least 600 bp that spanned 90% of both endonuclease and reverse transcriptase domains were considered as full-length elements.…”