2014 Annual Science Report
Massachusetts Institute of Technology Reporting | SEP 2013 – DEC 2014
Early Animals: Sensory Systems and Combinatorial Codes
Understanding the evolution of integrated sensory organs—such as the eyes, ears and nose that develop in concert on our heads—is fundamental to understanding animal complexity. These are the features that permit movement and the environmental responses that characterize animals. We examine understudied early branches of the animal family tree, with a focus on the jellyfish Aurelia, to understand how the genetic regulation of sensory organs is conserved in some cases and evolves in others. Comparison of developmental regulation reveals how similar gene networks can be differentially modified and deployed, permitting the evolution of complex sensory systems. Jellyfish provide an ideal study system for the examination of the evolution of such sensory systems in animal evolution, as they are the most basal branch the animal tree with multiple sensory modes, and these develop at multiple stages in a complex life history. This provides us the ability to compare and contrast within the broader cnidarian group to which jellyfish belong, and to the bilaterians, the broad group containing humans and most other animals. The application of genomic methods greatly enhances our ability to pursue these questions.
One perspective on the genetic control of sense-organ development centers around the concept of a combinatorial code, where expression of some genes is shared across multiple sensory structures, while the expression of other genes is specific to particular organs, and the particular combination is responsible for neural and sensory differentiation. In this context the combinatorial code permits the evolution and development of complex sensory features and neural architecture in animals. In this regard we are conducting a range of investigations on our organism of choice, the jellyfish Aurelia, as well as conducting studies that range across a broader suite of basal Metazoans.
Aurelia is of particular utility due to its position near the base of the animal tree, as well as its multiple life-history stages that each develop multiple distinct types of sensory structures. Our recent work on Aurelia involves a suite of stage specific comparisons across the life history using different methods. Using developmental markers of cell division combined with neuromuscular markers and transmission electron microscopy, we examined the development, and sensorymotor attributes of tentacles born in different life history stages. This work, to be submitted next month, advances our understanding of how one organism has evolved multiple distinct sensory appendages with distinct functions.
A more comprehensive examination has involved the transcriptomic study of the different life history stages. This has been quite revealing in terms of the suite of genes present in jellyfish relative to other cnidarian and bilaterian taxa, and in the differential expression between life history stages. We anticipate that this will lead to two separate publications. One will be based on broad differences between life history stages in differential expression and how that relates to the development of different sensory structures present. This exercise will provide a strong basis for a broad understanding of the genetic regulation in the different stages of development. A second publication will focus on the homeodomain composition and details of gene expression using in situ hybridization. This is of particular interest, as we have found jellyfish specific hoxgenes distinct from those in other Cnidaria and Bilateria.
One set of genes particularly relevant to the combinatorial code hypothesis is the POU family of regulatory genes. This past year we published a gene tree analysis (Gold et al. 2014) on the early radiation of this gene family in the Metazoa. We demonstrated support for a “neofunctionalization” model of POU gene duplication, whereby one of the duplicates retains the ancestral condition and function, while the other takes on new functional roles at the molecular level. This is an important analysis confirming the mechanism by which regulatory networks gain function.
Gold, D. A., Gates, R. D., & Jacobs, D. K. (2014). The Early Expansion and Evolutionary Dynamics of POU Class Genes. Molecular Biology and Evolution, 31(12), 3136–3147. doi:10.1093/molbev/msu243
Hartenstein, V., & Jacobs, D. (2013). Developmental Plasticity, Straight from the Worm’s Mouth. Cell, 155(4), 742–743. doi:10.1016/j.cell.2013.10.038
PROJECT MEMBERS:David Jacobs
RELATED OBJECTIVES:Objective 4.1
Earth's early biosphere.
Production of complex life.