Emergence of an evolutionary innovation: Gene expression differences associated with the transition between oviparity and viviparity

Abstract Our understanding of the evolution of complex biological traits is greatly advanced by examining taxa with intermediate phenotypes. The transition from oviparity (egg-laying) to viviparity (live-bearing) has occurred independently in many animal lineages, but there are few phenotypic intermediates. The lizard Saiphos equalis exhibits bimodal reproduction, with some viviparous populations, and other oviparous populations with long egg-retention, a rare trait where most of embryonic development occurs inside the mother prior to late ovipositioning. We posit that oviparous S. equalis represent an intermediate form between “true” oviparity and viviparity. We used transcriptomics to compare uterine gene expression in these two phenotypes, and provide a molecular model for the genetic control and evolution of reproductive mode. Many genes are differentially expressed throughout the reproductive cycle of both phenotypes, which have clearly different gene expression profiles overall. The differentially expressed genes within oviparous and viviparous individuals have broadly similar biological functions putatively important for sustaining embryos, including uterine remodelling, respiratory gas and water exchange, and immune regulation. These functional similarities indicate either that long egg-retention is an exaptation for viviparity, or might reflect parallel evolution of similar gravidity-related changes in gene expression in long egg-retention oviparity. In contrast, gene expression changes across the reproductive cycle of long egg-retaining oviparous S. equalis are dramatically different from those of “true” oviparous skinks (such as Lampropholis guichenoti), supporting our assertion that oviparous S. equalis exhibit an intermediate phenotype between “true” oviparity and viviparity

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RNase III-CLASH of multi-drug resistant Staphylococcus aureus reveals a regulatory mRNA 3′UTR required for intermediate vancomycin resistance

Treatment of methicillin-resistant Staphylococcus aureus infections is dependent on the efficacy of last-line antibiotics including vancomycin. Treatment failure is commonly linked to isolates with intermediate vancomycin resistance (termed VISA). These isolates have accumulated point mutations that collectively reduce vancomycin sensitivity, often by thickening the cell wall. Changes in regulatory small RNA expression have been correlated with antibiotic stress in VISA isolates however the functions of most RNA regulators is unknown. Here we capture RNA–RNA interactions associated with RNase III using CLASH. RNase III-CLASH uncovers hundreds of novel RNA–RNA interactions in vivo allowing functional characterisation of many sRNAs for the first time. Surprisingly, many mRNA–mRNA interactions are recovered and we find that an mRNA encoding a long 3′ untranslated region (UTR) (termed vigR 3′UTR) functions as a regulatory ‘hub’ within the RNA–RNA interaction network. We demonstrate that the vigR 3′UTR promotes expression of folD and the cell wall lytic transglycosylase isaA through direct mRNA–mRNA base-pairing. Deletion of the vigR 3′UTR re-sensitised VISA to glycopeptide treatment and both isaA and vigR 3′UTR deletions impact cell wall thickness. Our results demonstrate the utility of RNase III-CLASH and indicate that S. aureus uses mRNA-mRNA interactions to co-ordinate gene expression more widely than previously appreciated