Transcriptome-wide single nucleotide polymorphisms related to electric organ discharge differentiation among African weakly electric fish species.

Julia Canitz,Frank Kirschbaum,Ralph Tiedemann

doi:10.1371/journal.pone.0240812

Julia Canitz, Frank Kirschbaum + Show 1 more

Open Access

https://doi.org/10.1371/journal.pone.0240812

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Journal: PloS one	Publication Date: Oct 27, 2020
Citations: 2	License type: CC BY 4.0

Affiliation: University of Potsdam, Humboldt-Universität zu Berlin

Abstract

African weakly electric fish of the mormyrid genus Campylomormyrus generate pulse-type electric organ discharges (EODs) for orientation and communication. Their pulse durations are species-specific and elongated EODs are a derived trait. So far, differential gene expression among tissue-specific transcriptomes across species with different pulses and point mutations in single ion channel genes indicate a relation of pulse duration and electrocyte geometry/excitability. However, a comprehensive assessment of expressed Single Nucleotide Polymorphisms (SNPs) throughout the entire transcriptome of African weakly electric fish, with the potential to identify further genes influencing EOD duration, is still lacking. This is of particular value, as discharge duration is likely based on multiple cellular mechanisms and various genes. Here we provide the first transcriptome-wide SNP analysis of African weakly electric fish species (genus Campylomormyrus) differing by EOD duration to identify candidate genes and cellular mechanisms potentially involved in the determination of an elongated discharge of C. tshokwe. Non-synonymous substitutions specific to C. tshokwe were found in 27 candidate genes with inferred positive selection among Campylomormyrus species. These candidate genes had mainly functions linked to transcriptional regulation, cell proliferation and cell differentiation. Further, by comparing gene annotations between C. compressirostris (ancestral short EOD) and C. tshokwe (derived elongated EOD), we identified 27 GO terms and 2 KEGG pathway categories for which C. tshokwe significantly more frequently exhibited a species-specific expressed substitution than C. compressirostris. The results indicate that transcriptional regulation as well cell proliferation and differentiation take part in the determination of elongated pulse durations in C. tshokwe. Those cellular processes are pivotal for tissue morphogenesis and might determine the shape of electric organs supporting the observed correlation between electrocyte geometry/tissue structure and discharge duration. The inferred expressed SNPs and their functional implications are a valuable resource for future investigations on EOD durations.

Highlights

In closely related teleost fish, species-specific differences can be observed in morphology, behavior, reproduction, and communication [1,2,3,4]
66986804, 117994270, 41018678 and 99097520 high quality reads were used to assemble de novo the transcriptomes of C. compressirostris, C. tshokwe, C. tamandua and G. petersii, respectively
The identification of orthologous sequences among the four transcriptomes outputted a total number of 36285 orthogroups containing 16661 orthogroups present in all species of which 5284 were Single Copy Orthogroups (SCO)

Summary

Introduction

In closely related teleost fish, species-specific differences can be observed in morphology, behavior, reproduction, and communication [1,2,3,4]. These trait differences are often adaptive, especially if the species have evolved (or at least occur) in sympatry [5,6,7,8]. Either the anterior or the posterior face of electrocytes gives rise to several finger-like evaginations fusing in a stalk, serving as the interface to the electromotor neuron Those stalks can penetrate the electrocyte and occur as single or multiple stalk-systems. A significantly longer EOD (> 4ms) occurs in C. tshokwe and is assumed to be the derived character state within the genus Campylomormyrus (Fig 1) [22, 23]

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