Molecular paleoecology: using gene regulatory analysis to address the origins of complex life cycles in the late Precambrian

Abstract

SUMMARY Molecular paleoecology is the application of molecular data to test hypotheses made by paleoecological scenarios. Here, we use gene regulatory analysis to test between two competing paleoecological scenarios put forth to explain the evolution of complex life cycles. The first posits that early bilaterians were holobenthic, and the evolution of macrophagous grazing drove the exploitation of the pelagos by metazoan eggs and embryos, and eventually larvae. The alternative hypothesis predicts that early bilaterians were holopelagic, and new adult stages were added on when these holopelagic forms began to feed on the benthos. The former hypothesis predicts that the larvae of protostomes and deuterostomes are not homologous, with the implication that larval-specific structures, including the apical organ, are the products of convergent evolution, whereas the latter hypothesis predicts homology of larvae, specifically homology of the apical organ. We show that in the sea urchin, Strongylocentrotus purpuratus, the transcription factors NK2.1 and HNF6 are necessary for the correct spatial expression profiles of five different cilia genes. All of these genes are expressed exclusively in the apical plate after the mesenchyme-blastula stage in cells that also express NK2.1 and HNF6. In addition, abrogation of SpNK2.1 results in embryos that lack the apical tuft. However, in the red abalone, Haliotis rufescens, NK2.1 and HNF6 are not expressed in any cells that also express these same five cilia genes. Nonetheless, like the sea urchin, the gastropod expresses both NK2.1 and FoxA around the stomodeum and foregut, and FoxA around the proctodeum. As we detected no similarity in the development of the apical tuft between the sea urchin and the abalone, these molecular data are consistent with the hypothesis that the evolution of mobile, macrophagous metazoans drove the evolution of complex life cycles multiple times independently in the late Precambrian.

Neurogenic gene regulatory pathways in the sea urchin embryo

“…S4C′ versus D′); only a few cells continued to express Endo1, marking the location of the vegetal pole. The APD territory was at least partially retained, as evidenced by a contiguous patch of expression of Nk2.1, which is a driver of a separate regulatory pathway that constructs the apical tuft of cilia within the APD (Dunn et al, 2007) (Fig. S4E versus F and G).…”

The evolution of nervous system patterning: insights from sea urchin development

“…Six3 is necessary for development of the thickened columnar epithelial structure of the ANE and for the development of all neurons that develop there (Wei et al, 2009). FoxQ2 is also necessary for serotonergic neuron development, as well as for the expression of the transcription factor Nk2.1 (Yaguchi et al, 2008), which in turn controls the expression of a novel, ankryn repeat-containing protein (AnkAT) that is required for the formation of apical tuft cilia (Dunn et al, 2007;Yaguchi et al, 2010b). At the late mesenchyme blastula stage, cells expressing delta appear in the animal plate (Lapraz et al, 2009;Rottinger et al, 2006;Saudemont et al, 2010;Walton et al, 2006) and neuron number is controlled by lateral inhibition (Wei et al, 2011).…”

Origins of the other metazoan body plans: the evolution of larval forms

“…Other features (e.g. the apical plate with its ciliary tuft) have co-opted unrelated sets of regulatory genes in sea urchin versus mollusc larvae (Dunn et al 2007). Larval evolution would have been a build-up of features that would have diverted the ancestral course of development into two temporally distinct streams, one that first produced a feeding larva and a second stream that, from larval tissue, developed the juvenile adult.…”