Genomes of historical specimens reveal multiple invasions of LTR retrotransposons inDrosophila melanogasterpopulations during the 19^thcentury

Abstract

Transposable element invasions have a profound impact on the evolution of genomes and phenotype. It is thus an important open question on how often such TE invasions occur. Based on strains sampled at different times, previous work showed that four different TE families invaded D. melanogaster during the 20th century. Here we utilize the genomes of historical specimens to extend this work by another 100 years. We found that the LTR retrotransposons Blood, Opus and 412 spread in D. melanogaster in the 19th century. These invasions were found to constitute second waves, as degraded fragments were found for all three TEs. We show that two of the three invasions, Opus and 412, led to pronounced geographic heterogeneity, likely due to founder effects during the invasions. Finally, we identified species from the simulans complex as the likely origin of the TEs. In total, seven TE families invaded D. melanogaster during the last 200 years, increasing the genome size by 1.2 Mbp. Based on the analysis of strains and specimens sampled at different times, we provide a detailed timeline of TE invasions, making D. melanogaster the first organism where we could infer the invasion history of TEs during the last two centuries.

Spoink, a LTR retrotransposon, invadedD. melanogasterpopulations in the 1990s

“…3A). This is consistent with previous works suggesting that the P -element invaded D. melanogaster between 1950 and 1980 [Kidwell, 1983, Anxolabéhère et al, 1985, Bonnivard and Higuet, 1999, Scarpa et al, 2023]. Our data thus suggest that Spoink invaded D. melanogaster after the P -element invasion.…”

“…Previous work showed that at least seven TE families invaded D. melanogaster populations during the last two hundred years [Scarpa et al, 2023, Schwarz et al, 2021, Kidwell, 1983]. To explore whether additional, hitherto poorly characterised TEs could have invaded D. melanogaster , we investigated long-read assemblies of recently collected D. melanogaster strains [Rech et al, 2022] using a newly assembled repeat library [Chakraborty et al, 2021].…”

“…Previous work showed that the composition of TEs within a species may differ among geographic regions [Schwarz et al, 2021, Scarpa et al, 2023]. Such geographic heterogeneity could result from founder effects occurring during the geographic spread of a TE.…”

“…These small RNAs bind to PIWI clade proteins and mediate the degradation of TE transcripts and the formation of heterochromatin silencing the TE [Brennecke et al, 2007, Le Thomas et al, 2013, 2014a,b, Yamanaka et al, 2014, Andreev et al, 2022, Rangan et al, 2011]. However, while host defenses quickly adapt to new transposon invasions, TEs can escape silencing through horizontal transfer to new, defenseless, genomes [Peccoud et al, 2017, Scarpa et al, 2023, Kofler et al, 2015, Signor et al, 2023].…”

“…It was further realized that the I -element, Hobo and Tirant spread in D. melanogaster populations earlier than the P-element, between 1930 and 1960 [Kidwell, 1983, Periquet et al, 1989, Schwarz et al, 2021]. The genomes from historical D. melanogaster specimens collected about two hundred years ago, recently revealed that Opus, Blood , and 412 spread in D. melanogaster populations between 1850 and 1933 [Scarpa et al, 2023]. In total, it was suggested that seven TEs invaded D. melanogaster populations during the last two hundred years where one invasion (the P -element) was triggered by horizontal transfer from a species of the willistoni group and six invasions by horizontal transfer from the simulans complex [Schwarz et al, 2021, Scarpa et al, 2023, Loreto et al, 2008, Daniels et al, 1990, Simmons, 1992, Blumenstiel, 2019].…”