Massive Gene Loss and Function Shuffling in Appendicularians Stretch the Boundaries of Chordate Wnt Family Evolution

Abstract

Gene loss is a pervasive source of genetic variation that influences species evolvability, biodiversity and the innovation of evolutionary adaptations. To better understand the evolutionary patterns and impact of gene loss, here we investigate as a case study the evolution of the wingless (Wnt) family in the appendicularian tunicate Oikopleura dioica, an emergent EvoDevo model characterized by its proneness to lose genes among chordates. Genome survey and phylogenetic analyses reveal that only four of the thirteen Wnt subfamilies have survived in O. dioica—Wnt5, Wnt10, Wnt11, and Wnt16,—representing the minimal Wnt repertoire described in chordates. While the loss of Wnt4 and Wnt8 likely occurred in the last common ancestor of tunicates, representing therefore a synapomorphy of this subphylum, the rest of losses occurred during the evolution of appendicularians. This work provides the first complete Wnt developmental expression atlas in a tunicate and the first insights into the evolution of Wnt developmental functions in appendicularians. Our work highlights three main evolutionary patterns of gene loss: (1) conservation of ancestral Wnt expression domains not affected by gene losses; (2) function shuffling among Wnt paralogs accompanied by gene losses; and (3) extinction of Wnt expression in certain embryonic directly correlated with gene losses. Overall our work reveals that in contrast to “conservative” pattern of evolution of cephalochordates and vertebrates, O. dioica shows an even more radical “liberal” evolutionary pattern than that described ascidian tunicates, stretching the boundaries of the malleability of Wnt family evolution in chordates.

A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning

“…In summary, this provides a complex network of mutational protection, and thus the loss of one of these redundant/complementary Wnt factors (caused by either depletion of the gene, or regulatory changes) may not alter the development of the organism very much. Indeed, it has been shown that function-shuffling occurs regularly in Wnt genes, often associated with gene loss [ 52 , 56 , 84 ]. The latter, however, is not mandatory, especially when the gene is part of multiple GRNs.…”

Integrated analysis of Wnt signalling system component gene expression

“…This suggests that spatio-temporal intersection is not unique to the more complex gene family in the mouse. Evolutionary studies comparing Amphioxus and the tunicate Oikopleura dioica have suggested three modes of evolutionary change in the Wnt gene family namely, conservation of function, function shuffling and gene loss (Martí-Solans et al, 2021). It is possible that the co-expression of subdomains of different Wnts in the mouse reflects the operation of a conserved ancestral regulation, though not necessarily conservation of precise gene function, across different Wnts.…”

Variation of length and sequence of the nuclear ribosomal DNA internal transcribed spacer 1 supports “hermit-to-king” crab hypothesis

“…An alternative hypothesis is the loss of extensive genomic regions or chromosomes on which L-and M-type ITS1s are clustered. Adaptive phenotypic diversity due to gene loss (Olson 1999;Albalat and Cañestro 2016;Marti-Solans et al 2021) may have been associated with the morphological transformation of hermit crabs to king crabs. ochotensis, GT: Elassochirus cavimanus).…”