Goldfish phenomics reveals commonalities and a lack of universality in the domestication process for ornamentation

Abstract

Domestication process effects are manifold, affecting genotype and phenotype, and assumed to be universal in animals by part of the scientific community. While mammals and birds have been thoroughly investigated, from taming to intensive selective breeding, fish domestication remains comparatively unstudied. The most widely bred and traded ornamental fish species worldwide, the goldfish, underwent the effect of long-term artificial selection on differing skeletal and soft tissue modules through ornamental domestication. Here, we provide a global morphological analysis in this emblematic ornamental domesticated fish. We demonstrate that goldfish exhibit unique morphological innovations in whole-body, cranial, and sensory (Weberian ossicles and brain) anatomy compared to their evolutionary clade, highlighting a remarkable morphological disparity within a single species comparable to that of a macroevolutionary radiation. In goldfish, as in the case of dogs and pigeons in their respective evolutionary contexts, the most ornamented varieties are extremes in the occupied morphological space, emphasizing the power of artificial selection for nonadaptive traits. Using 21st century tools on a dataset comprising the 16 main goldfish breeds, 23 wild close relatives, and 39 cypriniform species, we show that Charles Darwin's expressed wonder at the goldfish is justified. There is a commonality of overall pattern in the morphological differentiation of domesticated forms selected for ornamental purposes, but the singularity of goldfish occupation and extension within (phylo)morphospaces, speaks against a universality in the domestication process.

Keywords: artificial selection; fish domestication; phenomics.

Figure 1.

Fully dichotomous phylogeny used in PCoA. We crafted the phylogeny based on the genera in our sample present in the robust molecular phylogeny of Stout et al. (2016), conserving branch lengths. We added goldfish and some Cyprininae to the tree based on the phylogenies of Tang et al. (2011) and Podlesnykh et al. (2015), duplicating the branch lengths of Gymnocypris from the phylogeny of Tang et al. (2011). We forced the dichotomy of incorporated taxa by following the phylogeny of Chen et al. (2020) and the diagrammatic genealogy of Smartt (2008). The production of this tree in addition to the tree shown in Supplementary Figure S2 is justified by the need to incorporate a fully resolved tree for PCoA. As a control test, we provide additional analyses without the incorporation of phylogeny (Supplementary Figure S3). Fish illustrations are not scaled, and references are available in Supplementary Table S7.

Figure 2.

Anatomical plate of virtual skeleton, swim bladder and Weberian ossicle models. (A) Lateral view of scaled skeleton with accentuated swim bladder and Weberian ossicles. (B) Dorsal view of scaled anterior and posterior swim bladder. (C) Dorsal (left) and lateral (right) view of scaled Weberian ossicles. Anatomical abbreviations following Bird and Hernandez (2007): Ant, anterior process; art, articular process; asc, ascending process; con, concha; man, manubrium; pst, posterior process; tra, transformator process.

Figure 3.

The new occupation of goldfish in the cypriniform phylomorphospace is mainly driven by the shape of the body and fins (N = 53). (A) Phylomorphospace (PCs 1–2 = 23.11%) from the PCoA performed on a distance matrix extracted from our cladistic matrix comprising 19 discretely coded morphological traits (Supplementary Table S2). The black dot in the phylomorphospace corresponds to the root of the tree. (B) Boxplot of the distance between each individual of each group (goldfish vs. other cypriniforms), resulting from the distance matrix. PERMANOVA rejected an approximately equal multivariate dispersion between goldfish and other cypriniforms (F = 16.665; P < 0.0001). (C) Dissimilarity neighbor-joining network covering all the variance from the distance matrix. Abbreviation: Cyprin., Cypriniformes. The color code follows that of Figure 1. Fish illustrations are not scaled, and references are available in Supplementary Table S7.

Figure 4.

Domestication impacts all neurocranial shape components, especially the orbit and supraoccipital crest. (A) 3D neurocranial phylomorphospace (PCs 1–3 = 59.6%; N = 84) from a PaCA, including goldfish, C. gibelio, and other cypriniforms (32 cyprinids + 7 danionids). Unscaled 3D meshes in lateral view were added to highlight the shape diversity expressed in the 3D phylomorphospace. The black dot corresponds to the nodes of the tree. (B) 3D neurocranial morphospace (PCs 1–3 = 63.8%; N = 49) from a PCA, focusing on goldfish and C. gibelio and including the morphological disparity analysis computed and compared using Procrustes variance. Neurocranial shape changes in lateral view between the most distant goldfish and C. gibelio on each PC of the morphospace are provided. The 3D meshes were superimposed and rendered transparent to highlight the vectors and the associated shape deformations. The five breeds projected on the PC1 correspond to the selected breeds for the brain volume comparisons. The color code follows that of Figure 1.

Figure 5.

Goldfish show a highly disparate shape for the Weberian ossicles—swim bladder complex compared to C. gibelio. (A) 3D Weberian ossicle morphospace (PCs 1–3 = 36.7%; N = 56) from a RCPCA associated with the morphological disparity expressed through Procrustes variances of goldfish and C. gibelio. Heat maps were used to illustrate the shape deformations of each Weberian ossicle from the consensual shape to every extreme of each PC. 3D meshes are unscaled and in dorsal view. The right side was duplicated from the left for visualization purposes. (B) Multivariate regression of the Weberian ossicle shape with the log swim bladder volume (N = 45). The dotted lines show the slopes of each group. Boxplots have been added to highlight the amount of shape and size variation in goldfish and C. gibelio. An example of the high diversity of swim bladders in goldfish compared to C. gibelio is provided. Unscaled specimens are shown in transparency and lateral view to reveal their swim bladder (3D models). The color code follows that of Figure 1. Abbreviations: SB, swim bladder; WO, Weberian ossicles.

Figure 6.

Domestication leads to a drastic reduction of the brain size in its entirety and regionally. (A) Overall brain anatomy at the same scale illustrated in lateral view for the goldfish closest to its wild counterparts, i.e., common goldfish, and one of the most distant, i.e., Bubble-eye breed. Brains show parcellated coloration to illustrate the different brain regions. (B) Histogram of relative brain volume and related relative regions volumes, with one being the closest relative to wild counterparts, i.e., common goldfish, and five being the most distant, i.e., Celestial breed (see Figure 4 for the five-breed selection). Total brain volume was standardized using neurocranial centroid size, while each brain region was standardized by total brain volume. Asterisks indicate brain region subject to distinct volume trends between common goldfish and other breeds. The color code in (B) follows the color code from (A). Fish illustrations are not scaled, and references are available in Supplementary Table S7.