Revelation of the Genetic Basis for Convergent Innovative Anal Fin Pigmentation Patterns in Cichlid Fishes

Abstract

Determining whether convergent novelties share a common genetic basis is vital to understanding the extent to which evolution is predictable. The convergent evolution of innovative anal fin pigmentation patterns in cichlid fishes is an ideal model for studying this question. Here, we focused on two patterns: 1) egg-spots, circular pigmentation patterns with different numbers, sizes and positions; and 2) the blotch, irregular pattern with no variation among species. How these two novelties originate and evolve remains unclear. Based on a thorough comparative transcriptomic and genomic analysis, we observed a common genetic basis with high evolutionary rates and similar expression levels between egg-spots and the blotch. But the associations of common genes with transcription factors and signalling pathways in the core gene network, as well as the integration of advantageous genes were observed specifically for egg-spots. Focusing on the whole transcriptomic level instead of limited numbers of candidate genes can explain the opposite conclusion between our study and the one from Santos et al. (2016), which suggested that no common genetic basis is shared between the blotch and egg-spots. Here, we propose that the re-use of the common genetic basis indicates important conservative functions (e.g., toolkit genes) for the origin of these convergent novel phenotypes, whereas independently evolved associations of common genes with transcription factors and signalling pathways (intrinsic factor) can free the evolution of egg-spots, and together with the integration of advantageous genes (extrinsic factor) can provide a clue to link egg-spots as a key innovation to the adaptive radiation in cichlid fishes. This hypothesis will further illuminate the mechanism of the origin and evolution of novelties in a broad sense.

Developmental and comparative transcriptomic identification of iridophore contribution to white barring in clownfish

“…Among the 86 genes more highly expressed in white skin than orange skin, fhl2a and fhl2b— already known to be expressed in iridophores (Santos et al, )—and gpnmb had higher expression in zebrafish iridophores than melanophores (Higdon et al, ). Apolipoprotein D ( apoD1a ) is expressed specifically in cichlids egg‐spots but its function in pigmentation, if any, has not been characterized (Gu & Xia, ). Finally, the gene with the second highest change in white skin was an ortholog to zebrafish gene ENSDARG00000055172 (Ensembl)/795494 (NCBI; Figure a) with no associated function in Ensembl, NCBI, or ZFIN databases.…”

Comparative transcriptomics reveals candidate carotenoid color genes in an East African cichlid fish

“…Enzymes of the short chain dehydrogenase/reductase SDR family (dhrs) catalyze the reversible oxidation/reduction of retinol and retinal [69]. Although their retinoid redox activity might suggest a function in the enzymatic conversion of carotenoids, dhrsx also deserves attention due to its association with xanthophore organization in the fins of cichlids and zebrafish [70,71]. We note, however, that qPCR detected dorsally elevated expression of dhrsx also in the white-barred population of T. duboisi, suggesting that the dorsoventral expression differences of dhrsx are not necessarily connected with carotenoids in the yellow-barred population.…”

Spotting genome-wide pigmentation variation in a brown trout admixture context

“…chromatophores; mainly melanophores, iridophores, leucophores and xanthophores) are distributed in the hypo- and the epidermis in fish, and mutational or other analyses allowed for increased understanding in the complex mechanisms of pigment cell fates during development and their resulting distribution (Kelsh et al, 2004, 2009; Kimura et al, 2014; Eom, Bain, Patterson, Grout, & Parichy, 2015; Nüsslein-Völlard & Singh, 2017; Parichy & Spiewak, 2015; Singh & Nüsslein-Völlard, 2015; Salis et al, 2018; Volkening 2020). Studies now extend to other fish species (Maan & Sfec, 2013; Irion & Nüsslein-Völlard, 2019) and to a large array of eco-evolutionary questions regarding the involvement of genes or regulatory pathways in fish pigmentation, its epistatic and pleiotropic nature, its modularity and its control, sexually antagonist selection or its role in speciation as well as the impact of whole-genome duplication that promoted the diversification of pigment cell lineages (Hultman, Bahary, Zon, & Johnson, 2007; Miller et al, 2007; Braasch, Brunet, Volff, & Schartl, 2009; Roberts, Ser & Kocher, 2009; Albertson et al, 2014; Santos et al 2014; Ceinos, Guillot, Kelsh, Cerdá-Reveter, & Rotlland, 2015; Yong, Peichel, & McKinnon, 2015; Gu & Xia 2017; Kimura, Takehana, & Naruse, 2017; Roberts, Moore, & Kocher, 2017; Sefc et al, 2017; Lorin, Brunet, Laudet, & Volff, 2018; Kratochwil et al, 2018; Nagao et al, 2018; Cal et al, 2019; Lewis et al, 2019; Kon et al, 2020; Liang, Gerwin, Meyer, & Kratochwil, 2020). An increasing number of studies engaged fish research in high-throughput genomic approach of pigmentation variation (guppy: Tripathi et al, 2009; three-spine stickleback: Greenwood et al, 2011; Malek, Boughman, Dworkin, & Peichel, 2012; cichlids: O’Quin, Drilea, Conte, & Kocher, 2013; Henning, Jones, Franchini, & Meyer, 2013; Henning, Lee, Franchini, & Meyer, 2014; Albertson et al, 2014; Zhu et al, 2016; Roberts et al 2017; koi carp: Xu et al, 2014; arowana: Bian et al, 2016; goldfish: Kon et al, 2020).…”