Chiropterans Are a Hotspot for Horizontal Transfer of DNA Transposons in Mammalia

Abstract

Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.

Keywords: echidna; endogenous retrovirus; fusogenic envelope protein; monotremes; platypus.

Fig. 1.

(A) Total transposable element accumulation, (B) DNA transposon accumulation within the last 50 My, and (C and D) box plots depicting ranges of total DNA transposon genome content in 37 chiropterans and 8 outgroup mammalians. High DNA TE mammals are defined as described in the main text as E. telfairi, M. talazaci, S. aquaticus, and C. indochinensis. Bat families are indicated by abbreviations left of species names and are as follows: Pt, Pteropodidae; Me, Megadermatidae; Cr, Craseonycteridae; Rh, Rhinolophidae; Hi, Hipposideridae; Ve, Vespertilionidae; Mi, Miniopteridae; Mol, Molossidae; No, Noctilionidae; Mor, Mormoopidae; and Ph, Phyllostomidae.

Fig. 2.

Violin plots of DNA transposon distributions by superfamily in bats. Distributions of (A) hAT, (B) piggyBac, (C) Tc-Mariner, and (D) Helitron elements within the last 50 My in 37 bat species. Species are arranged phylogenetically; bat families are indicated by abbreviations left of species names and are as follows: Pt, Pteropodidae; Me, Megadermatidae; Cr, Craseonycteridae; Rh, Rhinolophidae; Hi, Hipposideridae; Ve, Vespertilionidae; Mi, Miniopteridae; Mol, Molossidae; No, Noctilionidae; Mor, Mormoopidae; and Ph, Phyllostomidae.

Fig. 3.

Posterior distributions of group category (bats vs. nonbat eutherian mammals) on horizontal TE transfer counts. A constant of 1 was added to HTT counts for plotting to show the wide range of posterior estimates, which spans many orders of magnitude. For each coefficient: large dots show the median, thin lines show the 95% posterior probability, thick lines show the 66% posterior probability, and shaded curves show the posterior density of the estimates. Small dots show the observations on which the models were based.

Fig. 4.

Horizontal transfer of DNA transposons within Chiroptera. Inferred horizontal transfer (HT) events of 221 unique TEs from Tc-Mariner (circle), hAT (square), Helitron (hexagon), or piggyBac (pentagon) superfamilies are labeled on corresponding branches. Shape color indicates numerical range of putative HT events of a given branch: white, 1–4 elements; pink, 5–9; red, 10–15; and dark red, 16–20; the number of events was included within each marker. Phylogeny is scaled by estimated divergence times in millions of years (My). HT event branch assignment was inferred from presence/absence patterns and the element's average age. Phylogenetic relationships are based on Foley et al. (2022) and Amador et al. (2018); estimated divergence times were (supplementary table S10, Supplementary Material online) taken from TimeTree (Kumar et al. 2022).