Evidence for Non-neutral Evolution in a Sodium Channel Gene in African Weakly Electric Fish (Campylomormyrus, Mormyridae)

Paul, Christiane; Kirschbaum, Frank; Mamonékéné, Victor; Tiedemann, Ralph

doi:10.1007/s00239-016-9754-8

Cited by 19 publications

(20 citation statements)

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“…Several researchers have implicated the role of ion channels in the evolution of duration changes in mormyrid signals [53–57]. We did not find evidence of large changes in expression of potassium or sodium channels between short-duration P. sp.…”

Section: Discussioncontrasting

confidence: 84%

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The transcriptional correlates of divergent electric organ discharges inParamormyropselectric fish

Losilla

Gallant

2019

Preprint

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12Background: Understanding the genomic basis of phenotypic diversity can be greatly facilitated 13 by examining adaptive radiations with hypervariable traits. In this study, we focus on a rapidly 14 diverged species group of mormyrid electric fish in the genus Paramormyrops, which are 15 characterized by extensive phenotypic variation in electric organ discharges (EODs). The main 16 components of EOD diversity are waveform duration, complexity and polarity. Using an RNA-17 sequencing based approach, we sought to identify gene expression correlates for each of these 18 EOD waveform features by comparing 11 specimens of Paramormyrops that exhibit variation in 19 these features. 20Results: Patterns of gene expression among Paramormyrops are highly correlated, and 3,274 21 genes (16%) were differentially expressed. Using our most restrictive criteria, we detected 71-22 144 differentially expressed genes correlated with each EOD feature, with little overlap between 23 them. The predicted functions of several of these genes are related to extracellular matrix, cation 24 homeostasis, lipid metabolism, and cytoskeletal and sarcomeric proteins. These genes are of 25 significant interest given the known morphological differences between electric organs that 26 underlie differences in the EOD waveform features studied. 27Conclusions: In this study, we identified plausible candidate genes that may contribute to 28 phenotypic differences in EOD waveforms among a rapidly diverged group of mormyrid electric 29 fish. These genes may be important targets of selection in the evolution of species-specific 30 differences in mate-recognition signals.Understanding the genomic basis of phenotypic diversity is a major goal of evolutionary 33 biology [1]. Adaptive radiations and explosive diversification of species [2] are frequently 34 characterized by interspecific phenotypic differences in divergence of few, hypervariable 35 phenotypic traits [3][4][5][6]. Such systems offer exceptional advantages to study the genomic bases of 36 phenotypic diversity: they can provide replication under a controlled phylogenetic framework 37 [7], and couple ample phenotypic differentiation with relatively "clean" genomic signals between 38 recently diverged species [8]. Study of the genomic mechanisms underlying hypervariable 39 phenotypic traits has identified, in some cases relatively simple genetic architectures [9][10][11][12][13]. 40 More often, the genetic architecture underlying such traits can be complex and polygenic [14-41 17]. It has long been recognized that changes in gene expression can affect phenotypic 42 differences between species [18], and RNA-seq based approaches have greatly facilitated the 43 study of this relationship [19]. A growing number of studies have examined differences in gene 44 expression in phenotypic evolution (e.g., [19][20][21][22][23][24][25][26][27]). While these studies do not implicate 45 mutational causes, analysis of differential gene expression (DGE) can be a useful approach in 46 examining the ...

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Section: Discussioncontrasting

confidence: 84%

“…Recent studies in mormyrids [53–57] have adopted a candidate gene approach to examine the molecular basis of variation in EOD duration on macroevolutionary scales, implicating voltage gated sodium channels (e.g. scn4aa ) and potassium channels (e.g.…”

Section: Introductionmentioning

confidence: 99%

The transcriptional correlates of divergent electric organ discharges inParamormyropselectric fish

Losilla

Gallant

2019

Preprint

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“…The kcna7a potassium channel gene evolved rapidly preceding the adaptive radiation of the mormyrids. This is a similar pattern to that of a muscle-expressing sodium channel gene that also shifted its expression to the mormyrid EO (scn4aa) (36,37). The resulting amino acid substitutions in the S3-S4 linker in Kv1.7a contribute to biophysical changes that enable ultrabrief EODs.…”

Section: Discussionmentioning

confidence: 57%

Electrostatic Tuning of a Potassium Channel in Electric Fish

Swapna

Ghezzi

Markham

et al. 2017

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Abstract:Molecular and biophysical variation contributes to the evolution of adaptive phenotypes, particularly behavior, though it is often difficult to understand precisely how. The adaptively significant electric organ discharge behavior of weakly electric fish is the direct result of biophysical membrane properties set by ion channels. Here we describe a voltage-gated potassium channel gene in African mormyrid electric fishes, that is under positive selection and highly expressed in the electric organ. The channel produced by this gene shortens electric organ action potentials by activating quickly and at hyperpolarized membrane potentials. Surprisingly, the source of these unique properties is a derived patch of negatively charged amino acids in an extracellular loop near the voltage sensor. Further, we demonstrate that this portion of the channel functions differently in vertebrates than the generally accepted model based on the . CC-BY-NC-ND 4.0 International license It is made available under a (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/206243 doi: bioRxiv preprint first posted online Oct. 19, 2017; 2 shaker channel, and suggest a role for this loop in the evolutionary tuning of voltage-dependent channels.

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“…Several studies have reported increased evolutionary rates of scn4aa compared to scn4ab in electric fishes [38,42,68]. Hence, it would be interesting to elucidate whether the scnb isoforms, which modulate the Scna channels, would display similar patterns in their evolutionary rates following the evolution of EOs.…”

Section: Discussionmentioning

confidence: 99%

“…A phylogenetic analysis on the scnb isoforms was conducted following the general method of Paul et al [38]. Coding sequences of scn1b , scn2b and scn4b from E .…”

Section: Methodsmentioning

confidence: 99%

Voltage-Gated Na+ Channel Isoforms and Their mRNA Expression Levels and Protein Abundance in Three Electric Organs and the Skeletal Muscle of the Electric Eel Electrophorus electricus

et al. 2016

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This study aimed to obtain the coding cDNA sequences of voltage-gated Na+ channel (scn) α-subunit (scna) and β-subunit (scnb) isoforms from, and to quantify their transcript levels in, the main electric organ (EO), Hunter’s EO, Sach’s EO and the skeletal muscle (SM) of the electric eel, Electrophorus electricus, which can generate both high and low voltage electric organ discharges (EODs). The full coding sequences of two scna (scn4aa and scn4ab) and three scnb (scn1b, scn2b and scn4b) were identified for the first time (except scn4aa) in E. electricus. In adult fish, the scn4aa transcript level was the highest in the main EO and the lowest in the Sach’s EO, indicating that it might play an important role in generating high voltage EODs. For scn4ab/Scn4ab, the transcript and protein levels were unexpectedly high in the EOs, with expression levels in the main EO and the Hunter’s EO comparable to those of scn4aa. As the key domains affecting the properties of the channel were mostly conserved between Scn4aa and Scn4ab, Scn4ab might play a role in electrogenesis. Concerning scnb, the transcript level of scn4b was much higher than those of scn1b and scn2b in the EOs and the SM. While the transcript level of scn4b was the highest in the main EO, protein abundance of Scn4b was the highest in the SM. Taken together, it is unlikely that Scna could function independently to generate EODs in the EOs as previously suggested. It is probable that different combinations of Scn4aa/Scn4ab and various Scnb isoforms in the three EOs account for the differences in EODs produced in E. electricus. In general, the transcript levels of various scn isoforms in the EOs and the SM were much higher in adult than in juvenile, and the three EOs of the juvenile fish could be functionally indistinct.

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Evidence for Non-neutral Evolution in a Sodium Channel Gene in African Weakly Electric Fish (Campylomormyrus, Mormyridae)

Cited by 19 publications

References 77 publications

The transcriptional correlates of divergent electric organ discharges inParamormyropselectric fish

The transcriptional correlates of divergent electric organ discharges inParamormyropselectric fish

Electrostatic Tuning of a Potassium Channel in Electric Fish

Voltage-Gated Na+ Channel Isoforms and Their mRNA Expression Levels and Protein Abundance in Three Electric Organs and the Skeletal Muscle of the Electric Eel Electrophorus electricus

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