Less, but more: new insights from appendicularians on chordate Fgf evolution and the divergence of tunicate lifestyles.

Abstract

The impact of gene loss on the diversification of taxa and the emergence of evolutionary innovations remains poorly understood. Here, our investigation on the evolution of the Fibroblast Growth Factors (FGFs) in appendicularian tunicates as a case study reveals a scenario of "less, but more" characterized by massive losses of all Fgf gene subfamilies, except for the Fgf9/16/20 and Fgf11/12/13/14, which in turn underwent two bursts of duplications. Through phylogenetic analysis, synteny conservation, and gene and protein structure, we reconstruct the history of appendicularian Fgf genes, highlighting their paracrine and intracellular functions. Exhaustive analysis of developmental Fgf expression in Oikopleura dioica allow us to identify four associated evolutionary patterns characterizing the "less, but more" conceptual framework: conservation of ancestral functions; function shuffling between paralogs linked to gene losses; innovation of new functions after the duplication bursts; and function extinctions linked to gene losses. Our findings allow us to formulate novel hypotheses about the impact of Fgf losses and duplications on the transition from an ancestral ascidian-like biphasic lifestyle to the fully free-living appendicularians. These hypotheses include massive co-options of Fgfs for the development of the oikoblast and the tail fin; recruitment of Fgf11/12/13/14s into the evolution of a new mouth, and their role modulating neuronal excitability; the evolutionary innovation of an anterior tail FGF signaling source upon the loss of retinoic acid signaling; and the potential link between the loss of Fgf7/10/22 and Fgf8/17/18 and the loss of drastic metamorphosis and tail absorption in appendicularians, in contrast to ascidians.