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bioRxiv · 10.1101/2024.08.01.605096

Substantial hierarchical reductions of genetic and morphological traits in the evolution of rotiferan parasites

Herlyn, H.·Hembrom, A. A.·Tosar, J. P.·Mauer, K. M.·Schmidt, H.·Dezfuli, B. S.·Bachmann, L.·Sarkies, P.·Peterson, K. J.·Fromm, B.
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Abstract

O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=189 SRC="FIGDIR/small/605096v2_ufig1.gif" ALT="Figure 1"> View larger version (30K): org.highwire.dtl.DTLVardef@469ecborg.highwire.dtl.DTLVardef@6330f4org.highwire.dtl.DTLVardef@22faf6org.highwire.dtl.DTLVardef@8a6704_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical abstractC_FLOATNO C_FIG During the last 800 million years of evolution animals radiated into a vast range of diversity of species and disparity of forms and lifestyles. The process involved a near hierarchical increase in complexity from life forms with few cell types to organisms with many hundreds of cell-types. However, neither genome size nor number of protein-coding genes can explain these differences and their biological basis remains elusive. Yet, recent studies have suggested that the evolution of complexity is closely linked to the acquisition of a class of protein coding gene-regulators called microRNAs. In a regressive approach, to investigate the association between loss of organismal complexity and microRNAs, we here studied Syndermata, an invertebrate group including free-living rotifers (Monogononta, Bdelloidea), the epibiotic Seisonidea and the endoparasitic Acanthocephala. Genomic, transcriptomic and morphological characterization and comparisons across 25 syndermatan species revealed a strong correlation between loss of microRNAs, loss of protein-coding genes and decreasing morphological complexity. The near hierarchical loss extends to [~]85% loss of microRNAs and a [~]50% loss of BUSCO genes in the endoparasitic Acanthocephala, the most reduced group we studied. Together, the loss of [~]400 protein-coding genes and [~]10 metazoan core gene losses went along with one microRNA family loss. Furthermore, the loss of [~]4 microRNA families or [~]34 metazoan core genes associated with one lost morphological feature. These are the first quantitative insights into the regulatory impact of microRNAs on organismic complexity as a predictable consequence in regressive evolution of parasites.

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Herlyn, H., Hembrom, A. A., Tosar, J. P., Mauer, K. M., Schmidt, H., Dezfuli, B. S., Bachmann, L., Sarkies, P., Peterson, K. J., Fromm, B.. 2024-08-04. Substantial hierarchical reductions of genetic and morphological traits in the evolution of rotiferan parasites. https://doi.org/10.1101/2024.08.01.605096

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