Pronounced expression of extracellular matrix proteoglycans regulated by Wnt pathway underlies the parallel evolution of lip hypertrophy in East African cichlids
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eLife assessment
In this important study, the authors have partially revealed the mechanism behind lip thickening in cichlid fishes, which has evolved independently across three lakes in Africa. To explore this phenomenon, the authors utilized histological comparison, proteomics, and transcriptomics, all of which are well suited for their objectives. With convincing evidence, this contribution holds significant value for the field.
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Abstract
Cichlid fishes inhabiting the East African Great Lakes, Victoria, Malawi, and Tanganyika, are textbook examples of parallel evolution, as they have acquired similar traits independently in each of the three lakes during the process of adaptive radiation. In particular, “hypertrophied lip” has been highlighted as a prominent example of parallel evolution. However, the underlying molecular mechanisms remain poorly understood. In this study, we conducted an integrated comparative analysis between the hypertrophied and normal lips of cichlids across three lakes based on histology, proteomics, and transcriptomics. Histological and proteomic analyses revealed that the hypertrophied lips were characterized by enlargement of the proteoglycan-rich layer, in which versican and periostin proteins were abundant. Transcriptome analysis revealed that the expression of extracellular matrix-related genes, including collagens, glycoproteins and proteoglycans, was higher in hypertrophied lips, regardless of their phylogenetic relationships. In addition, the Wnt signaling pathway, which is involved in promoting proteoglycan expression, was highly expressed in both the juvenile and adult stages of hypertrophied lips. Our comprehensive analyses showed that hypertrophied lips of the three different phylogenetic origins can be explained by similar proteomic and transcriptomic profiles, which may provide important clues into the molecular mechanisms underlying phenotypic parallelisms in East African cichlids.
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eLife assessment
In this important study, the authors have partially revealed the mechanism behind lip thickening in cichlid fishes, which has evolved independently across three lakes in Africa. To explore this phenomenon, the authors utilized histological comparison, proteomics, and transcriptomics, all of which are well suited for their objectives. With convincing evidence, this contribution holds significant value for the field.
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Reviewer #1 (Public Review):
Summary:
Machii et al. reported a possible molecular mechanism underlying the parallel evolution of lip hypertrophy in African cichlids. The multifaceted approach taken in this manuscript is highly valued, as it uses histology, proteomics, and transcriptomics to reveal how phylogenetically distinct thick-lips have evolved in parallel. Findings from histology and proteomics connected to wnt signaling through the transcriptome are very exciting.
Strengths:
There is consistency between the results and it is possible to make a strong argument from the results.
Weaknesses:
The authors do not discuss based on genomic information; the genomes of the cichlids from the three lakes have been decoded and are therefore available. However, indeed, the species in Lake Tanganyika and Lake Malawi/Victoria are genetically …
Reviewer #1 (Public Review):
Summary:
Machii et al. reported a possible molecular mechanism underlying the parallel evolution of lip hypertrophy in African cichlids. The multifaceted approach taken in this manuscript is highly valued, as it uses histology, proteomics, and transcriptomics to reveal how phylogenetically distinct thick-lips have evolved in parallel. Findings from histology and proteomics connected to wnt signaling through the transcriptome are very exciting.
Strengths:
There is consistency between the results and it is possible to make a strong argument from the results.
Weaknesses:
The authors do not discuss based on genomic information; the genomes of the cichlids from the three lakes have been decoded and are therefore available. However, indeed, the species in Lake Tanganyika and Lake Malawi/Victoria are genetically distant from each other, so a comparative genome analysis would not have yielded the results presented here. I recommend adding such a discussion to the Discussion.
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Reviewer #2 (Public Review):
I have carefully reviewed the manuscript titled "Pronounced expression of extracellular matrix proteoglycans regulated by Ant pathway underlies the parallel evolution of lip hypertrophy in East African cichlids." I commend the authors for their work on elucidating the mechanism underlying lip thickening that has evolved in parallel across three lakes in Africa.
The use of histological comparison, proteomics, and transcriptomics methods to investigate this phenomenon is commendable and adds depth to the study. The findings indicate that the overexpression of proteoglycans is the cause of lip thickening and provides valuable insights into the evolutionary process.
I found the writing style to be clear and the explanations provided are easy to understand. Overall, I did not identify any significant issues with …
Reviewer #2 (Public Review):
I have carefully reviewed the manuscript titled "Pronounced expression of extracellular matrix proteoglycans regulated by Ant pathway underlies the parallel evolution of lip hypertrophy in East African cichlids." I commend the authors for their work on elucidating the mechanism underlying lip thickening that has evolved in parallel across three lakes in Africa.
The use of histological comparison, proteomics, and transcriptomics methods to investigate this phenomenon is commendable and adds depth to the study. The findings indicate that the overexpression of proteoglycans is the cause of lip thickening and provides valuable insights into the evolutionary process.
I found the writing style to be clear and the explanations provided are easy to understand. Overall, I did not identify any significant issues with the manuscript.
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