Comparative Transcriptomics Reveals Distinct Patterns of Gene Expression Conservation through Vertebrate Embryogenesis

Abstract

Despite life’s diversity, studies of variation often remind us of our shared evolutionary past. Abundant genome sequencing and analyses of gene regulatory networks illustrate that genes and entire pathways are conserved, reused, and elaborated in the evolution of diversity. Predating these discoveries, 19th-century embryologists observed that though morphology at birth varies tremendously, certain stages of vertebrate embryogenesis appear remarkably similar across vertebrates. In the mid to late 20th century, anatomical variability of early and late stage embryos and conservation of mid-stages embryos (the ‘phylotypic’ stage) was named the hourglass model of diversification. This model has found mixed support in recent analyses comparing gene expression across species possibly owing to differences in species, embryonic stages, and gene sets compared. We compare 186 microarray and RNA-seq data sets covering embryogenesis in six vertebrate species. We use an unbiased clustering approach to group stages of embryogenesis by transcriptomic similarity and ask whether gene expression similarity of clustered embryonic stages deviates from a null expectation. We characterize expression conservation pattern of each gene at each evolutionary node after correcting for phylogenetic non-independence. We find significant enrichment of genes exhibiting early conservation, hourglass, late conservation patterns in both microarray and RNA-seq data sets. Enrichment of genes showing patterned conservation through embryogenesis indicates diversification of embryogenesis may be temporally constrained. However, the circumstances under which each pattern emerges remain unknown and require both broad evolutionary sampling and systematic examination of embryogenesis across species.

Quantitative proteome dynamics across embryogenesis in a model chordate

“…Cross-species embryonic development is typically aligned at the transcriptome level. 48 , 49 , 50 , 51 , 53 , 55 We therefore used developmental proteomes to establish stage correspondences between Ciona and Xenopus species throughout embryogenesis. We identified 7,636 one-to-one orthologs at the gene level ( Tables S8 and S9 ).…”

“…The evolution of gene expression and its role in morphological innovations have been studied primarily by comparative transcriptomics. 48 , 49 , 50 , 51 These studies point toward a 'phylotypic period’ in vertebrates, whereby gene expression is most similar across different species during mid-embryogenesis or pharyngula stage, the “hourglass” model. 52 However, comparisons with non-vertebrate chordates such as tunicates and cephalochordates are not entirely consistent with the hourglass.…”

“… 58 Several studies stress limitations of simplistic pairwise comparisons, robust testing of null hypotheses, and the challenge in balancing phylogenetic distances, which can be too short among closely related species or too extensive when the comparisons are made between vertebrates and invertebrates or across multiple phyla. 51 , 53 , 58 …”

Quantitative proteome dynamics across embryogenesis in a model chordate

“…Haeckel proposed that embryonic development recapitulates evolutionary trajectories (Haeckel 1866). While this theory is no longer accepted, more recent studies investigating the phylotypic period across species have generated conflicting results when based solely on transcriptome data and when limited to short phylogenetic distances within vertebrates or long distances spanning invertebrates to vertebrates (Chan et al 2021;Uesaka et al 2022). While some studies support the existence of a mid-embryonic period with maximal similarity in gene expression, in line with the hourglass model, others propose an inverted hourglass model, highlighting higher conservation of gene expression in the early and late developmental phases (Levin et al 2016a;Marlétaz et al 2018a;Hu et al 2017a;Schrimpf et al 2009a;Laurent et al 2010a).…”

Transcriptome Analysis Provides Insights into Copulation, Fertilization, and Gestation in Sebastes schlegelii

“…Such studies have revealed genes and pathways involved in steroid regulation, vitellogenesis, lipid droplet synthesis, oocyte development, and maturation [ 3 , 4 , 5 , 6 ]. More research on embryogenesis during gestation in females has been carried out in mammals and other viviparous species [ 7 , 8 , 9 ]. However, research on viviparous teleosts is limited [ 10 ].…”