Abstract

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.

Highlights

  • Transposons are a major component of metazoan genomes, making up between 24% and 56% of squamate genomes (Pasquesi et al 2018)

  • To identify potential horizontal transposon transfer (HTT) events which may have occurred since the transition of elapids to a marine habitat, we looked for transposons identified in A. laevis that were not present in genome assemblies of its closest sequenced terrestrial relatives, Notechis scutatus and Pseudonaja textilis

  • For the majority of the seven subfamilies, the most similar LINE was present in a teleost fish, indicating either that the LINEs were repeatedly lost from all other tetrapods following their divergence from teleost fish 400 Ma, or the subfamilies were horizontally transferred into sea snakes and sea kraits following their divergence from terrestrial relatives

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Summary

Introduction

Transposons are a major component of metazoan genomes, making up between 24% and 56% of squamate genomes (Pasquesi et al 2018). HTT of DNA transposons and LTR retrotransposons appears to be more common, yet many examples of HTT of non-LTR retrotransposons (LINEs) have been described (Peccoud et al 2018). These include transfers of RTE-BovBs between multiple distant lineages (Ivancevic et al 2018), of AviRTEs between birds and parasitic nematodes (Suh et al 2016), and of Rex elements between teleost fish (Volff et al 2000; Zhang et al 2020). Previous studies in Drosophila found HTT to increase following colonization of new habitats due to exposure to new species (Biemont et al 1999; Vieira et al 2002)

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