Evidence for Active Maintenance of Phylotranscriptomic Hourglass Patterns in Animal and Plant Embryogenesis

Abstract

The developmental hourglass model has been used to describe the morphological transitions of related species throughout embryogenesis. Recently, quantifiable approaches combining transcriptomic and evolutionary information provided novel evidence for the presence of a phylotranscriptomic hourglass pattern across kingdoms. As its biological function is unknown it remains speculative whether this pattern is functional or merely represents a nonfunctional evolutionary relic. The latter would seriously hamper future experimental approaches designed to test hypotheses regarding its function. Here, we address this question by generating transcriptome divergence index (TDI) profiles across embryogenesis of Danio rerio, Drosophila melanogaster, and Arabidopsis thaliana. To enable meaningful evaluation of the resulting patterns, we develop a statistical test that specifically assesses potential hourglass patterns. Based on this objective measure we find that two of these profiles follow a statistically significant hourglass pattern with the most conserved transcriptomes in the phylotypic periods. As the TDI considers only recent evolutionary signals, this indicates that the phylotranscriptomic hourglass pattern is not a rudiment but possibly actively maintained, implicating the existence of some linked biological function associated with embryogenesis in extant species.

Convergent eusocial evolution is based on a shared reproductive groundplan plus lineage-specific plastic genes

“…Furthermore, adding extraneous genomes effectively dilutes the database, such that more similarity is needed to pass an E-value threshold. Because we included only a sample of non-hymenopteran genomes, we were therefore able to stringently identify orthologs (E-value 10 -10 in comparison to a typical value of 10 -5 ) 81 and accurately place them along the hymenopteran phylogeny.…”

Adaptive evolution of animal proteins over development: support for the Darwin selection opportunity hypothesis of Evo-Devo

“…Despite the repeated observation that late development is highly divergent for diverse genomic properties (sequence evolution, duplication, gene age, expression divergence) in diverse animal species (Roux and Robinson-Rechavi 2008;Domazet-Loso and Tautz 2010;Kalinka et al 2010;Irie and Kuratani 2011;Levin et al 2012;Piasecka et al 2013;Drost et al 2015;Liu and Robinson-Rechavi 2017), the underlying evolutionary forces driving such a pattern remain obscure. The "developmental constraint" hypothesis suggests that this high divergence is due to relaxed purifying selection, whereas Darwin's "selection opportunity" hypothesis proposes stronger positive selection (as discussed in Artieri et al 2009;Kalinka and Tomancak 2012 Artieri et al 2009;Kalinka et al 2010).…”

“…Based on recent genomic studies, both models have some level of molecular support. Some studies support the early conservation model (Roux and Robinson-Rechavi 2008;Artieri et al 2009), while most recent ones support the hourglass model (Kalinka et al 2010;Irie and Kuratani 2011;Levin et al 2012;Quint et al 2012;Drost et al 2015;Hu et al 2017;Zalts and Yanai 2017). And in fact the two models may not be mutually exclusive (Piasecka et al 2013;Liu and Robinson-Rechavi 2017).…”

Transcriptomes of plant gametophytes have a higher proportion of rapidly evolving and young genes than sporophytes

“…Studies in vertebrates (zebrafish) and insects (Drosophila melanogaster) confirmed this hypothesis because genes expressed during the phylotypic stage were more conserved and less rapidly evolving than genes expressed in other stages of development (Domazet-Lo so and Tautz 2010; Kalinka et al 2010). Although plants do not have a clear morphologically defined phylotypic stage, a transcriptomic hourglass was also postulated for the model plant Arabidopsis thaliana because old and slowly evolving genes contribute disproportionally to the overall transcriptome during early stages of embryo development (Quint et al 2012;Drost et al 2015), but see Piasecka et al (2013).…”