Ascidians present a striking dichotomy between conserved phenotypes and divergent genomes: embryonic cell lineages and gene expression patterns are conserved between distantly related species. Much research has focused on Ciona or Halocynthia spp. but development in other ascidians remains poorly characterized. In this study, we surveyed the multipotent myogenic B7.5 lineage in Molgula spp. Comparisons to the homologous lineage in Ciona revealed identical cell division and fate specification events that result in segregation of larval, cardiac, and pharyngeal muscle progenitors. Moreover, the expression patterns of key regulators are conserved, but cross-species transgenic assays uncovered incompatibility, or ‘unintelligibility’, of orthologous cis-regulatory sequences between Molgula and Ciona. These sequences drive identical expression patterns that are not recapitulated in cross-species assays. We show that this unintelligibility is likely due to changes in both cis- and trans-acting elements, hinting at widespread and frequent turnover of regulatory mechanisms underlying otherwise conserved aspects of ascidian embryogenesis.
When two species have features that look similar, this may be because the features arise by the same processes during development. Other features may look similar yet develop by different mechanisms. ‘Developmental system drift’ refers to the process where a physical feature remains unaltered during evolution, but the underlying pathway that controls its development is changed. However, to date, there have been only a few experimental studies that support this idea.
Ascidians—also commonly known as sea squirts—are vase-like marine creatures, which start off as tadpole-like larvae that swim around until they find a place to settle down and attach themselves. Once attached, the sea squirts lose the ability to swim and start feeding, typically by filtering material out of the seawater. Sea squirts and their close relatives are the invertebrates (animals without backbones) that are most closely related to all vertebrates (animals with backbones), including humans. Furthermore, although different species of sea squirt have almost identical embryos, their genomes are very different.
Stolfi et al. have now studied whether developmental system drift may have occurred during the evolution of ascidians, by analyzing different species of sea squirt named Molgula and Ciona. Stolfi et al. compared the genomes of Molgula and Ciona and studied the expression of genes in the cells that give rise to the heart and the muscles of the head. As an embryo develops, specific genes are switched on or off, and these patterns of gene activation were broadly identical in the two species of sea squirt examined.
Enhancers are sequences of DNA that control when and how a gene is switched on. Given the similarities between the development of heart and head muscle cells in the different sea squirts, Stolfi et al. looked to see if the mechanisms of gene expression, and therefore the enhancers, were also conserved. Unexpectedly, this was not the case. When enhancers from Molgula were introduced into Ciona (and vice versa), these sequences were unable to switch on gene expression—thus enhancers from one sea squirt species could not function in the other.
Stolfi et al. conclude that the developmental systems may have drifted considerably during evolution of the sea squirts, in spite of their nearly identical embryos. This reinforces the view that different paths can lead to the formation of similar physical features.