Open and closed evolutionary paths for drastic morphological changes, involving serial gene duplication, sub-functionalization and selection

et al. 2019

Developmental Dynamics

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Background Twin‐tail ornamental goldfish have “bifurcated median fins,” a peculiar morphology known to be caused by a mutation in the chdA gene. However, several ambiguities regarding the development of the phenotype remain due to a paucity of detailed observations covering the entire developmental timeframe. Results Here, we report a detailed comparative description of embryonic and postembryonic development for two representative twin‐tail ornamental goldfish strains and single‐tail common goldfish. Our observations reveal a polymorphic developmental process for bifurcated median fins; disrupted axial skeletal development at early larval stages; and modified bilateral location of the pelvic fin. Conclusions Variations in development of bifurcated median fins and disrupted axial skeletal patterns reflect how artificial selection for adult morphological features influenced molecular developmental mechanisms during the domestication of twin‐tail ornamental goldfish. The polymorphic appearance of bifurcated median fins also implies that, unlike previously proposed hypotheses, the development of these structures is controlled by molecular mechanisms independent of those acting on the pelvic fin. Our present findings will facilitate further study of how modifications of preexisting developmental systems may contribute to novel morphological features. Developmental Dynamics 248:251–283, 2019. © 2019 The Authors. Developmental Dynamics published by Wiley Periodicals, Inc. on behalf of American Association of Anatomists.

Section: Discussionmentioning

confidence: 91%

Embryonic and postembryonic development of the ornamental twin‐tail goldfish

et al. 2019

Developmental Dynamics

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“…In fact, the injection of MOs that target either of the szl paralogues in single‐tail common‐goldfish embryos was sufficient to reproduce the bifurcated caudal fin and its primodia (Figures and e,f; Supporting Information Figure S1). Therefore, the szl paralogues are not functionally redundant and cannot rescue each other, unlike other paralogous gene sets that exhibit partial redundancy, incomplete non‐functionalization, or neo‐functionalization (Figure ; Abe et al., ; Force et al., ; Innan & Kondrashov, ; Rastogi & Liberles, ; Sémon & Wolfe, ). Our results suggest that the absence of szl ‐type twin‐tail goldfish in domesticated populations is not due to buffering mechanisms between szl paralogues.…”

Section: Discussionmentioning

confidence: 99%

“…In the common carp, it was reported that the chd gene paralogues are expressed at early embryonic stages in a completely overlapping manner. Thus, the depletion of a single chd gene paralogue did not produce any notable phenotypes at late larval stages (Abe et al., ; Sémon & Wolfe, ). In this report, we examine the presence/absence of szl gene paralogues and whether the depletion of the szl gene can cause the twin‐tail morphology in goldfish.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

J Exp Zool Pt B

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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.

“…On the other hand, our previous study reported a conservative evolutionary process for the chdA and chdB genes in common carp, based on their gene expression patterns. Moreover, an equivalent stop codon allele for chdA has not been found in our previous studies or publicly available genomic data for the common carp (Abe et al, , ; Xu et al, ). These major differences lead us to ask the question of why the chdA and chdB paralogues have evolved in such a different manner in the two closely related lineages of goldfish and common carp, which shared a genome duplication and were both domesticated.…”

Section: Discussionmentioning

confidence: 60%

“…These major differences lead us to ask the question of why the chdA and chdB paralogues have evolved in such a different manner in the two closely related lineages of goldfish and common carp, which shared a genome duplication and were both domesticated. Furthermore, our analyses could not sufficiently explain why the branch length of the goldfish chdB gene is longer in comparison with some other chordin genes in the phylogenetic tree (Abe et al, , ; Figure B). More specifically, our molecular developmental genetics led us to conclude that while the chdA gene highly contributed to morphological evolution, the nucleotide sequence of chdB evolved faster than that of chdA , suggesting the conservative nature of chdA gene sequence.…”

Section: Discussionmentioning

confidence: 66%

A novel allele of the goldfish chdB gene: Functional evaluation and evolutionary considerations

et al. 2018

J Exp Zool Pt B

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The twin tail of ornamental goldfish is known to be caused by a nonsense mutation in one chordin paralogue gene. Our previous molecular studies in goldfish revealed that the ancestral chordin gene was duplicated, creating the chdA and chdB genes, and the subsequent introduction of a stop codon allele in the chdA gene ( chdA E127X ) caused the twin‐tail morphology. The chdA E127X allele was positively selected by breeders, and the allele was genetically fixed in the ornamental twin‐tail goldfish population. However, little is known about the evolutionary history of the chdB paralogue, begging the question: are there the functionally distinct alleles at the chdB locus, and if so, how did they evolve? To address these questions, we conducted molecular sequencing of the chdB gene from five different goldfish strains and discovered two alleles at the chdB gene locus; the two alleles are designated chdB 1 and chdB 2 . The chdB 1 allele is the major allele and was found in all investigated goldfish strains, whereas the chdB 2 allele is minor, having only been found in one twin‐tail strain. Genetic analyses further suggested that these two alleles are functionally different with regard to survivability ( chdB 1 > chdB 2 ). These results led us to presume that in contrast to the chdA locus, the chdB locus has tended to be eliminated from the population. We also discuss how the chdB 2 allele was retained in the goldfish population, despite its disadvantageous function. This study provides empirical evidence of the long‐term retention of a disadvantageous allele under domesticated conditions.