Title:

Gene Family Dynamics at the Earliest Branches of Metazoa

As knowledge of diverse organisms’ genic repertoire grows, the scientific community has had cause to reevaluate the role of gene loss as a major influence in shaping the evolutionary dynamics of animals. Some metazoan lineages in particular, such as Porifera, lack many complex traits that nearly all other animals possess including a nervous system, gut, or bodily symmetry. Sponges may have always lacked these traits and represent a state of ancestral simplicity, or it is possible that they formerly possessed complex traits in common with other animals and have since lost them, reflecting a degeneration of that complexity. Here, we examine the evolutionary dynamics of gene family gain and loss near the root of the Metazoa tree and show that sponges previously possessed the genic repertoire of other early-branching animal lineages. They lose gene families associated with tissue-grade multicellularity, development and morphology, and nervous systems, while gaining families that could help facilitate interactions with a microbial community. We find that gene family gains typically ascribed to the ancestral metazoan node are divided between that and the node leading to Porifera+ParaHoxozoa. Our results demonstrate that sponges previously possessed the gene families necessary to have complex traits similar to other animals, but have since lost them, and these findings will ameliorate concerns on the phylogenetic position of sponges that are based on organismal complexity.

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