Transcriptome analysis reveals the genetic basis underlying the seasonal development of keratinized nuptial spines in Leptobrachium boringii

Abstract

Background: The expression of sexually selected traits often varies with populations' breeding cycles in many animals. The elucidation of mechanisms underlying the expression of such traits is a research topic in evolutionary biology; however, the genetic basis of the seasonal development of their expression remains unknown. Male Leptobrachium boringii develop keratinized nuptial spines on their upper jaw during the breeding season that fall off when the breeding season ends. To illuminate the genetic basis for the expression of this trait and its seasonal development, we assessed the de novo transcriptome for L. boringii using brain, testis and upper jaw skin and compared gene expression profiles of these tissues between two critical periods of the spine growth cycle. Results: We identified 94,900 unigenes in our transcriptome. Among them, 2,131 genes were differentially expressed between the breeding period when the spines developed and the post-breeding period when the spines were sloughed. An increased number of differentially expressed genes (DEGs) were identified in the upper jaw skin compared with the testis and brain. In the upper jaw skin, DEGs were mainly enriched in cytosolic part, peptidase inhibitor activity and peptidase regulator activity based on GO enrichment analysis and in glycolysis/gluconeogenesis, ribosome biogenesis in eukaryotes and retinol metabolism based on KEGG enrichment analysis. In the other two tissues, DEGs were primarily involved in the cell cycle, DNA replication and melatonin production. Specifically, insulin/insulin-like growth factor and sex steroid hormone-related DEGs were identified in the upper jaw skin, indicating. The expression variation of IGF2 and estrogen-related genes may be the main factors regulating the seasonal development of the spines. Conclusions: Our study provides a list of potential genes involved in the regulation of seasonal development of nuptial spines in L. boringii. This is the first transcriptome survey of seasonally developed sexually selected traits for non-model amphibian species, and candidate genes provided here may provide valuable information for further studies of L. boringii.