The evolutionary history of mariner elements in stalk-eyed flies reveals the horizontal transfer of transposons from insects into the genome of the cnidarian Hydra vulgaris

Abstract

The stalk-eyed flies (Diopsidae, Diptera) are a family of approximately 100 species of calypterate dipterans, characterised by extended head capsules. Species within the family have previously been shown to possess six subfamilies of mariner transposons, with nucleotide substitution patterns suggesting that at least two subfamilies are currently active. The vertumnana subfamily has been shown to have been involved in a horizontal transfer event involving Diopsidae and a second dipteran family in the Tephritidae. Presented here are cloned and sequenced mariner elements from three further diopsid species, in addition to a bioinformatic analysis of mariner elements identified in transcriptomic and genomic data from the genus Teleopsis. The newly identified mariner elements predominantly fall into previously recognised subfamilies, however the publicly available Teleopsis data also revealed a novel subfamily. Three of the seven identified subfamilies are shown to have undergone horizontal transfer, two of which appear to involve diopsid donor species. One recipient group of a diopsid mariner is the Bactrocera genus of tephritid flies, the transfer of which was previously proposed in an earlier study of diopsid mariner elements. The second horizontal transfer, of the mauritiana subfamily, can be traced from the Teleopsis genus to the cnidarian Hydra vulgaris. The mauritiana elements are shown to be active in the recipient H. vulgaris and transposase expression is observed in all body tissues examined in both species. The increased diversity of diopsid mariner elements points to a minimum of four subfamilies being present in the ancestral genome. Both vertical inheritance and stochastic loss of TEs have subsequently occurred within the diopsid radiation. The TE complement of H. vulgaris contains at least two mariner subfamilies of insect origin. Despite the phylogenetic distance between donor and recipient species, both subfamilies are shown to be active and proliferating within H. vulgaris.

Fig 1. Representative phylogeny of diopsid species.

Cladogram highlighting the relationships between the diopsid species involved in this study, based upon Kotrba and Balke [28] and Kotrba et al [29].

Fig 2. Maximum likelihood phylogeny of diopsid mariner sequences.

The phylogeny was constructed from 480 aligned nucleotide positions using the GTRCAT model, and estimated nucleotide frequencies. Values for mlBP and biPP are shown above and below the branches respectively. 100% mlBP and 1.00 biPP are both denoted by “*”. Values <70% mlBP and <0.97 biPP are denoted by “-”. The scale bar represents the number of substitutions per site. Individual mariner subfamilies are bracketed and colour-coded.

Fig 3. Maximum likelihood phylogeny of the mosellana subfamily.

The phylogeny was constructed from 1032 aligned nucleotide positions using the GTRCAT model, and estimated nucleotide frequencies. The mosellana elements are bracketed and rooted with tnpase sequences from the irritans and mellifera subfamilies. Values for mlBP and biPP are shown above and below the branches respectively. Diopsid sequences are shown in purple, other dipteran sequences are shown in light blue. Dark blue sequences are from hymenopteran hosts, pink sequences from lepidopteran hosts, the orange sequence is from an archaeognath host and light green sequences are from copepod hosts. The brown sequence is from a hydrozoan host and the mustard sequence from a fish host. The outgroup sequences are from the irritans subfamily (Semar1 and Temar2.2) and the mellifera subfamily (Temar3.1). 100% mlBP and 1.00 biPP are both denoted by “*”. Values <50% mlBP and <0.70 biPP are denoted by “-”. The scale bar represents the number of substitutions per site.

Fig 4. Maximum likelihood phylogeny of the vertumnana subfamily.

The phylogeny was constructed from 510 aligned nucleotide positions using the GTRCAT model and estimated nucleotide frequencies. Support values are shown in the same format as Fig 3.

Fig 5. Maximum likelihood phylogeny of the mauritiana subfamily.

The phylogeny was constructed from 492 aligned nucleotide positions using the GTRCAT model and estimated nucleotide frequencies. Support values are shown in the same format as Fig 3.