On the contingent nature of satellite DNA evolution

Background The full catalogue of satellite DNA (satDNA) within a same genome constitutes the satellitome. The Library Hypothesis predicts that satDNA in relative species reflects that in their common ancestor, but the evolutionary mechanisms and pathways of satDNA evolution have never been analyzed for full satellitomes. We compare here the satellitomes of two Oedipodine grasshoppers ( Locusta migratoria and Oedaleus decorus ) which shared their most recent common ancestor about 22.8 Ma ago. Results We found that about one-third of their satDNA families (near 60 in every species) showed sequence homology, and were grouped into 12 orthologous superfamilies. The turnover rate of consensus sequences was extremely variable among the 20 orthologous family pairs analyzed in both species. The satDNAs shared by both species showed poor association with sequence signatures and motives frequently argued as functional, except for short inverted repeats allowing short dyad symmetries and non-B DNA conformations. Orthologous satDNAs frequently showed different FISH pattern at both intra- and interspecific levels. We defined indices of homogenization and degeneration, and quantified the level of incomplete library sorting between species. Conclusions Our analyses revealed that satDNA degenerates through point mutation and rejuvenates through partial turnovers caused by massive tandem duplications (the so-called satDNA amplification). Remarkably, satDNA amplification increases homogenization, at intragenomic level, and diversification between species, thus constituting the basis for concerted evolution. We suggest a model of satDNA evolution by means of recursive cycles of amplification, degeneration, and rejuvenation, leading to mostly contingent evolutionary pathways where concerted evolution emerges promptly after lineages split. ### Competing Interest Statement The authors have declared no competing interest. * B-pattern : Banded pattern (pattern in FISH analyses) CEI: Concerted Evolution Index CI : Confidence Interval CTR : Consensus Turnover Rate dG: Gibbs free energy DIVPEAK: Divergence Peak FISH : Fluorescence In Situ Hybridization ILibS: Incomplete Library Sorting K2P : Kimura Two-Parameter (substitution model) Lmi: Locusta migratoria NS-pattern : No signal pattern (in FISH analyses) MAL : Maximum Array Length (observed in MinIon reads of L. migratoria ) MST : Minimum Spanning Tree Ode : Oedaleus decorus OSF : Orthologous Superfamily RL: Repeat Landscape RPS : Relative peak size RUL: Repeat Unit Length satDNA: satellite DNA SF: Superfamily TSI : Tandem Structure Index VIF : Variance inflation factors