Eye Degeneration and Loss of otx5b Expression in the Cavefish Sinocyclocheilus tileihornes

Zushi Huang,Fanwei Meng,Tom Titus,John H Postlethwait

doi:10.1007/s00239-019-09901-8

Zushi Huang, Fanwei Meng + Show 2 more

Open Access

https://doi.org/10.1007/s00239-019-09901-8

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Abstract

Cave animals possess remarkable phenotypes associated with existence in their dark environments. The Chinese cavefish Sinocyclocheilus tileihornes shows substantial eye degeneration, a trait shared by most cave species. The extent to which independent evolution of troglomorphic traits uses convergent molecular genetic mechanisms is as yet unknown. We performed transcriptome-wide gene expression profiling in S. tileihornes eyes and compared results with those from the closely related surface species S. angustiporus and an independently derived congeneric cavefish, S. anophthalmus. In total, 52.85 million 100 bp long paired-end clean reads were generated for S. tileihornes, and we identified differentially expressed genes between the three possible pairs of species. Functional analysis of genes differentially expressed between S. tileihornes and S. angustiporus revealed that phototransduction (KEGG id: dre04744) was the most significantly enriched pathway, indicating the obvious differences in response to captured photons between the cavefish S. tileihornes and the surface species S. angustiporus. Analysis of key genes regulating eye development showed complete absence of otx5b (orthodenticle homolog 5) expression in S. tileihornes eyes, probably related to degradation of rods, but normal expression of crx (cone-rod homeobox). The enriched pathways and Otx5 are involved in phototransduction, photoreceptor formation, and regulation of photoreceptor-related gene expression. Unlike the S. tileihornes reported here, S. anophthalmus has reduced crx and otx5 expression. These results show that different species of cavefish within the same genus that independently evolved troglodyte characteristics can have different genetic mechanisms of eye degeneration.

Highlights

Blind cavefish provide an excellent model for the study of the genetic mechanisms for the evolution of developmental change
In addition to the thin retinas and more sparsely populated photoreceptors found in cavefish S. anophthalmus and S. tileihornes (Stil) relative to that of surface species S. angustiporus (Sang), we found that the arrangement of rods in cavefish S. tileihornes (Stil) was disorganized (Meng et al 2013b)
We constructed a combined Sinocyclocheilus transcriptome from the new S. tileihornes assembly plus the previous transcriptome assemblies of S. anophthalmus and S. angustiporus that contained 59,631 contigs with N50 of 1318, of which 41,134 contigs matched 15,649 zebrafish genes (GRCz11) (Table S1). 36.98 million (61.65%) S. angustiporus reads, 26.68 million (57.33%) S. anophthalmus read and 30.06 million (56.88%) S. tileihornes reads mapped to the combined Sinocyclocheilus reference transcriptome using Bowtie 2 software

Summary

Introduction

Blind cavefish provide an excellent model for the study of the genetic mechanisms for the evolution of developmental change. To help address this question, we used RNA-seq to perform transcriptome sequencing for examination of gene expression levels in the eyes of three Sinocyclocheilus species. We identified differences in eye transcriptomes of S. tileihornes compared with that of the surface species S. angustiporus and another cavefish, S. anophthalmus.

Results

Conclusion