An intronic transposon insertion associates with a trans-species color polymorphism in Midas cichlid fishes

Kratochwil, Claudius F.; Kautt, Andreas F.; Nater, Alexander; Härer, Andreas; Liang, Yipeng; Henning, Frederico; Meyer, Axel

doi:10.1038/s41467-021-27685-8

Cited by 25 publications

(25 citation statements)

References 41 publications

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“…Another family of fish in which the genetic basis and transcriptional correlates of several pigment pattern and coloration phenotypes have been thoroughly investigated are cichlid fishes. The phenotypes that have been studied from a genetic and/or transcriptomic perspective include egg spot patterns (Henning & Meyer, 2012; Salzburger et al, 2007; Santos et al, 2014), morphological color change (Henning et al, 2013; Kautt et al, 2020; Kratochwil et al, 2022), blotch patterns (Roberts et al, 2017, 2009), general differences in pigment cell distribution (Albertson et al, 2014), yellow, carotenoid‐based coloration (Ahi et al, 2020), and vertical bar patterns (Gerwin et al, 2021; Liang et al, 2020). Another common phenotype that has been investigated molecularly are horizontal stripe patterns in cichlids.…”

Section: Introductionmentioning

confidence: 99%

Comparative ontogenetic and transcriptomic analyses shed light on color pattern divergence in cichlid fishes

Kratochwil

Liang

Gerwin

et al. 2022

Evolution and Development

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Stripe patterns are a striking example for a repeatedly evolved color pattern. In the African adaptive radiations of cichlid fishes, stripes evolved several times independently. Previously, it has been suggested that regulatory evolution of a single gene, agouti‐related‐peptide 2 (agrp2), explains the evolutionary lability of this trait. Here, using a comparative transcriptomic approach, we performed comparisons between (adult) striped and nonstriped cichlid fishes of representatives of Lake Victoria and the two major clades of Lake Malawi (mbuna and non‐mbuna lineage). We identify agrp2 to be differentially expressed across all pairwise comparisons, reaffirming its association with stripe pattern divergence. We therefore also provide evidence that agrp2 is associated with the loss of the nonstereotypic oblique stripe of Mylochromis mola. Complementary ontogenetic data give insights into the development of stripe patterns as well as vertical bar patterns that both develop postembryonically. Lastly, using the Lake Victoria species pair Haplochromis sauvagei and Pundamilia nyererei, we investigated the differences between melanic and non‐melanic regions to identify additional genes that contribute to the formation of stripes. Expression differences—that most importantly also do not include agrp2—are surprisingly small. This suggests, at least in this species pair, that the stripe phenotype might be caused by a combination of more subtle transcriptomic differences or cellular changes without transcriptional correlates. In summary, our comprehensive analysis highlights the ontogenetic and adult transcriptomic differences between cichlids with different color patterns and serves as a basis for further investigation of the mechanistic underpinnings of their diversification.

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Section: Introductionmentioning

confidence: 99%

Comparative ontogenetic and transcriptomic analyses shed light on color pattern divergence in cichlid fishes

Kratochwil

Liang

Gerwin

et al. 2022

Evolution and Development

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“…Among these are the elements of the peripheral nervous system, pigment cells and craniofacial cartilages and bones (Douarin and Kalcheim, 1999). The NC-derived phenotypes that received most attention in cichlids are their distinctive pigmentation patterns (Albertson et al, 2014; Brzozowski et al, 2012; Hendrick et al, 2019; Kratochwil et al, 2018, 2022; Liang et al, 2020; Roberts et al, 2017; Santos et al, 2014), and the dramatic variation in craniofacial morphologies, associated with the divergent trophic strategies (Albertson and Kocher, 2006; Conith et al, 2018; Powder and Albertson, 2016; Powder et al, 2014, 2015).…”

Section: Introductionmentioning

confidence: 99%

Morphological and temporal variation in early embryogenesis contributes to species divergence in Malawi cichlid fishes

Marconi

Yang

McKay

et al. 2022

Preprint

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The cichlid fishes comprise the largest extant vertebrate family and are the quintessential example of rapid "explosive" adaptive radiations and phenotypic diversification. Despite low genetic divergence, East African cichlids harbour a spectacular intra- and interspecific morphological diversity, including the hyper-variable, neural crest (NC)-derived traits such as colouration and craniofacial skeleton. Although the genetic and developmental basis of these phenotypes has been investigated, understanding of when, and specifically how early, in ontogeny species-specific differences emerge, remains limited. Since adult traits often originate during embryonic development, the processes of embryogenesis could serve as a potential source of species-specific variation. Consequently, we compared the features of embryogenesis between three Malawi cichlid species - Astatotilapia calliptera, Tropheops sp. 'mauve' and Rhamphochromis sp. 'chilingali' - representing a wide spectrum of variation in pigmentation and craniofacial morphologies. Our results showed fundamental differences in multiple aspects of embryogenesis that could underlie interspecific divergence in adult adaptive traits. Firstly, we identified variation in the somite number and signatures of temporal variation, or heterochrony, in the rates of somite formation. The heterochrony was also evident within and between species throughout ontogeny, up to the juvenile stages. Finally, the identified interspecific differences in the development of pigmentation and craniofacial cartilages, present at the earliest stages of their overt formation, provide compelling evidence that the species-specific trajectories begin divergence during early embryogenesis, potentially during somitogenesis and NC development. Altogether, our results expand our understanding of fundamental cichlid biology and provide new insights into the developmental origins of vertebrate morphological diversity.

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“…The mechanism controlling morphological polymorphism of Midas cichlid is assumed to be monogenic (Thomas, 1976;Henning et al, 2013), and the putative serine/threonine kinase gene (stk) has been considered as the molecular basis for differentiation of the dark/gold phenotypes (Kautt et al, 2020). However, more recently a new defined gene "goldentouch" may also contribute to the division of dark/gold types (Kratochwil et al, 2022). A comparative transcriptomic analysis revealed significant transcriptional changes of the core genes involved in the melanosomal pathway, potentially acting as the main factors to affect the dark/gold differentiation (Henning et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

An Updated Genome Assembly Improves Understanding of the Transcriptional Regulation of Coloration in Midas Cichlid

Li²,

Liu³

et al. 2022

Front. Mar. Sci.

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Midas cichlid (Amphilophus citrinellus), a popular aquarium fish, attracts extensive attention from worldwide biologists mainly due to its morphological polymorphism (dark versus gold). Continuous efforts have therefore been paid to address mechanisms of its coloration variants, while it is far away from the detailed illustration of a clear regulatory network. Some limits may come from the absence of a high-quality genome assembly and a relatively accurate gene set. In this study, we sequenced about 149 Gb of nucleotide sequences of Midas cichlid, generating a genome assembly with a total size of 933.5 Mb, which exhibits a good genome continuity with a contig N50 of 10.5 Mb. A total of 25,911 protein-coding genes were annotated and about 90% completeness was achieved, which helps to build a good gene pool for understanding expressional differences of color variation. With the assistance of the final gene set, we identified a total of 277 differential expressional genes (DEGs), of which 97 up- and 180 downregulated were determined in dark-vs-gold comparisons. Two protein-protein interaction (PPI) networks were constructed from these DEGs, and three key functional modules were classified. Hub genes within each module were evaluated, and we found that the third key module contains tyrp1b, oca2, pmela, tyr, and slc24a5, which were previously proven to be associated with melanin formation. Two downregulated DEGs (myl1 and pgam2) in the first key module may be involved in muscle movement and spermatogenesis, implying that certain side effects could result from the morphological polymorphism. The first key module, consisting of proteins encoded by upregulated DEGs that were associated with MAPK signaling, Toll-like receptor signaling, and gonadotropin-releasing hormone pathways, may contribute to a negative upstream regulation or downstream influence on melanin biosynthesis. Taken together, our new genome assembly and gene annotation of Midas cichlid provide a high-quality genetic resource for biological studies on this species, and the newly identified key networks and hub genes in dark-vs-gold comparisons enhance our understanding of the transcriptional regulatory mechanisms underlying coloration changes not only in Midas cichlid but also in other fishes from freshwater to marine ecosystems.

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An intronic transposon insertion associates with a trans-species color polymorphism in Midas cichlid fishes

Cited by 25 publications

References 41 publications

Comparative ontogenetic and transcriptomic analyses shed light on color pattern divergence in cichlid fishes

Comparative ontogenetic and transcriptomic analyses shed light on color pattern divergence in cichlid fishes

Morphological and temporal variation in early embryogenesis contributes to species divergence in Malawi cichlid fishes

An Updated Genome Assembly Improves Understanding of the Transcriptional Regulation of Coloration in Midas Cichlid

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