Rapid evolutionary diversification of theflamencolocus across simulans cladeDrosophilaspecies

Abstract

Maintaining genomic integrity through suppression of transposable elements (TEs) is paramount to organismal fitness. In D. melanogaster flamenco is the master regulator of TE suppression, preventing TEs from moving from the somatic support cells of the ovary to the germline. It is thought to operate as a trap, suppressing TEs upon their transposition into the locus, with a high representation of recent horizontally transferred TEs. We find that in the simulans clade flamenco has undergone physical and functional diversification. In D. simulans flamenco has duplicated and diverged from its original, maintaining no synteny within the locus but conserving its promotor. In D. simulans and D. mauritiana, flamenco acts as a dual stranded cluster with ping pong signals in some tissues. This expansion in function has been accompanied by an increase in the number of multicopy elements, as expected for regions operating as dual stranded clusters. In addition, we find that in D. simulans presence of a TE in either flamenco or a germline cluster, may be necessary for suppression of a TE but it may not be entirely sufficient. This physical and functional diversity of flamenco in the simulans clade redefines our understanding of this locus.

Unistrand piRNA clusters are an evolutionarily conserved mechanism to suppress endogenous retroviruses across theDrosophilagenus

“…Our data hint towards a conversion over time of unistrand loci into dual-strand clusters, or vice versa, although it could also reflect a propensity to repeatedly form piRNA clusters at specific genomic locations, likely those with low recombination rate and low selective pressure 46 . In support of the conversion model, signatures of germline flam expression have been observed in D. simulans and D. mauritiana 52 . Additionally, we observed germline expression towards the 3’ ends of D. erecta and D. yakuba flam -syntenic clusters.…”

Rapid evolution of promoters from germline-specifically expressed genes including transposon silencing factors

“…Somatic follicle cells only feature unistrand piRNA clusters, such as flamenco ( flam ), and exclusively produce piRNAs via a Zucchini (Zuc)-dependent biogenesis mechanism that takes place on the mitochondria surface involving Armitage (Armi), Papi, Vreteno (Vret), Gasz, Daedalus (Daed), Minotaur (Mino), Shutdown (Shu), and Sister of Yb (SoYb) (Fig. 1A) [3, 12, 13]. Licensing of flam for piRNA production takes place upstream, at so-called Yb-bodies [1, 12].…”

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

“…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].…”

“…This horizontal transfer allows TEs to colonize the genomes of novel species [Zhang et al, 2020, Zanni et al, 2013, Signor et al, 2023, Schaack et al, 2010, Peccoud et al, 2017]. The first well-documented instance of horizontal transfer of a TE was the P -element, which spread from D. willistoni to D. melanogaster [Daniels et al, 1990].…”