An alternative evolutionary pathway for the twin‐tail goldfish via szl gene mutation

Abstract

The twin‐tail of ornamental goldfish provides unique evolutionary evidence that the highly conserved midline localization of axial skeleton components can be changed by artificial selection. This morphological change is known to be caused by a nonsense mutation in one of the recently duplicated chordin genes, which are key players in dorsal–ventral (DV) patterning. Since all of the multiple twin‐tail ornamental goldfish strains share the same mutation, it is reasonable to presume that this mutation occurred only once in domesticated goldfish. However, zebrafish with mutated szl gene (another DV patterning‐related gene) also exhibit twin‐tail morphology and higher viability than dino/chordin‐mutant zebrafish. This observation raises the question of whether the szl gene mutation could also reproduce the twin‐tail morphology in goldfish. Here we show that goldfish have at least two subfunctionalized szl genes, designated szlA and szlB, and depletion of these genes in single‐fin goldfish was able to reproduce the bifurcated caudal fin found in twin‐tail ornamental goldfish. Interestingly, several phenotypes were observed in szlA‐depleted fish, while low expressivity of the twin‐tail phenotype was observed in szlB‐depleted goldfish. Thus, even though szl gene mutations may produce twin‐tail goldfish, these szl gene mutations might not be favorable for selection in domestic breeding. These results highlight the uniqueness and rarity of mutations that are able to cause large‐scale morphological changes, such as a bifurcated axial skeleton, with high viability and expressivity in natural and domesticated populations.

The Genetic Basis of Morphological Diversity in Domesticated Goldfish

“…We compared the amino acid sequences of candidate gene paralogs (Data S1P). We observed that the paralogs S and L show clearly higher identities (80%-92% amino acid identity) than those between paralogs a and b (44%-56% amino acid identity), reflecting the ancient history of Cs4R and Ts3R [11][12][13][14][15], consistent with previous studies [62][63][64][65]. We also compared the expression of these paralogs (Data S1O).…”

Pleiotropic functions of chordin gene causing drastic morphological changes in ornamental goldfish

“…In fact, this interpretation allows us to explain why the majority of our F2 backcross progenies consistently exhibited mutant phenotypes in dorsal, anal, and caudal fins (Supplementary Tables S1 , S2 ). Moreover, previous reports on szl -depleted goldfish are consistent with this interpretation 18 , 33 . Depletion of szl gene expression in goldfish embryos leads to the dorsal-finless phenotype, which is related to the chordin gene 33 .…”

“…Moreover, previous reports on szl -depleted goldfish are consistent with this interpretation 18 , 33 . Depletion of szl gene expression in goldfish embryos leads to the dorsal-finless phenotype, which is related to the chordin gene 33 . Although the detailed molecular developmental mechanisms of the dorsal fin disappearance are still unknown, it is certain that the depletion of this gene disrupts dorsal–ventral patterning to generate the dorsal-finless phenotype in the goldfish 33 .…”

Pleiotropic functions of chordin gene causing drastic morphological changes in ornamental goldfish

“…In fact, this interpretation allows us to explain why the majority of our F2 backcross progenies consistently exhibited mutant phenotypes in dorsal, anal, and caudal fins (Supplementary Table S1 and S2). Moreover, previous reports on szl-depleted goldfish are consistent with this interpretation 18,33 . Depletion of szl gene expression in goldfish embryos leads to the dorsal-finless phenotype, which is related to the chordin gene.…”

“…Depletion of szl gene expression in goldfish embryos leads to the dorsal-finless phenotype, which is related to the chordin gene. Importantly, the depletion of this gene disrupts dorsal-ventral patterning to generate the dorsal-finless phenotype in the goldfish 33 .…”