Evolutionary fate and implications of retrocopies in the African coelacanth genome

Abstract

Background: The coelacanth is known as a "living fossil" because of its morphological resemblance to its fossil ancestors. Thus, it serves as a useful model that provides insight into the fish that first walked on land. Retrocopies are a type of novel genetic element that are likely to contribute to genome or phenotype innovations. Thus, investigating retrocopies in the coelacanth genome can determine the role of retrocopies in coelacanth genome innovations and perhaps even water-to-land adaptations.

Results: We determined the dS values, dN/dS ratios, expression patterns, and enrichment of functional categories for 472 retrocopies in the African coelacanth genome. Of the retrocopies, 85-355 were shown to be potentially functional (i.e., retrogenes). The distribution of retrocopies based on their dS values revealed a burst pattern of young retrocopies in the genome. The retrocopy birth pattern was shown to be more similar to that in tetrapods than ray-finned fish, which indicates a genomic transformation that accompanied vertebrate evolution from water to land. Among these retrocopies, retrogenes were more prevalent in old than young retrocopies, which indicates that most retrocopies may have been eliminated during evolution, even though some retrocopies survived, attained biological function as retrogenes, and became old. Transcriptome data revealed that many retrocopies showed a biased expression pattern in the testis, although the expression was not specifically associated with a particular retrocopy age range. We identified 225 Ensembl genes that overlapped with the coelacanth genome retrocopies. GO enrichment analysis revealed different overrepresented GO (gene ontology) terms between these "retrocopy-overlapped genes" and the retrocopy parent genes, which indicates potential genomic functional organization produced by retrotranspositions. Among the 225 retrocopy-overlapped genes, we also identified 46 that were coelacanth-specific, which could represent a potential molecular basis for coelacanth evolution.

Conclusions: Our study identified 472 retrocopies in the coelacanth genome. Sequence analysis of these retrocopies and their parent genes, transcriptome data, and GO annotation information revealed novel insight about the potential role of genomic retrocopies in coelacanth evolution and vertebrate adaptations during the evolutionary transition from water to land.

Fig. 1

Venn diagram of the unique and common retrocopies among different categories. Red refers to retrocopies that overlap with Ensembl genes. Yellow refers to retrocopies with intact ORFs. Green refers to retrocopies with evidence of transcription. Blue refers to retrocopies with dN/dS ratios significantly <0.5

Fig. 2

The dS distribution of the 472 retrocopies in the genome of the African coelacanth

Fig. 3

Dot plot of the dN/dS ratios with the dS values for each of the 472 retrocopies

Fig. 4

Percentages of retrocopies with different indications of functionality in each dS bin, distributed according to the increase in dS values. The red line corresponds to the right Y-axis and represents the number of retrocopies. The lines in black, grey, blue and green correspond to the left Y-axis and represent the percentages of retrocopies showing intact ORFs, dN/dS ratios significantly <0.5,overlap with Ensembl genes and transcriptional evidence, respectively

Fig. 5

Mean expression levels of retrocopies in different dS bins. Expression levels were measured as log(FPKM + 1) values

Fig. 6

Mean expression frequency for retrocopies in different dS bins