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Genes linked to species diversity in a sexually dimorphic communication signal in electric fish

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Abstract

Sexually dimorphic behaviors are often regulated by androgens and estrogens. Steroid receptors and metabolism are control points for evolutionary changes in sexual dimorphism. Electric communication signals of South American knifefishes are a model for understanding the evolution and physiology of sexually dimorphic behavior. These signals are regulated by gonadal steroids and controlled by a simple neural circuit. Sexual dimorphism of the signals varies across species. We used transcriptomics to examine mechanisms for sex differences in electric organ discharges (EODs) of two closely related species, Apteronotus leptorhynchus and Apteronotus albifrons, with reversed sexual dimorphism in their EODs. The pacemaker nucleus (Pn), which controls EOD frequency (EODf), expressed transcripts for steroid receptors and metabolizing enzymes, including androgen receptors, estrogen receptors, aromatase, and 5α-reductase. The Pn expressed mRNA for ion channels likely to regulate the high-frequency activity of Pn neurons and for neuromodulator and neurotransmitter receptors that may regulate EOD modulations used in aggression and courtship. Expression of several ion channel genes, including those for Kir3.1 inward-rectifying potassium channels and sodium channel β1 subunits, was sex-biased or correlated with EODf in ways consistent with EODf sex differences. Our findings provide a basis for future studies to characterize neurogenomic mechanisms by which sex differences evolve.

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Abbreviations

11KT:

11-Ketotestosterone

11β-HSD:

11β-Hydroxysteroid dehydrogenase

17β-HSD:

17β-Hydroxysteroid dehydrogenase

5αDHT:

5α-Dihydrotestosterone

5HT:

Serotonin

AVT:

Arginine vasotocin

AR:

Androgen receptor

ER:

Estrogen receptor

BUSCO:

Benchmarking universal single-copy orthologs

CP-PPn:

Central posterior-prepacemaker nucleus

E2:

Estradiol

EOD:

Electric organ discharge

EODf:

Electric organ discharge frequency

GFR:

Gradual frequency rise

GO:

Gene ontology

GPER:

G-protein coupled estrogen receptor

GSI:

Gonadosomatic index

IHW:

Independent hypothesis weighted

JAR:

Jamming avoidance response

KChIP:

K+ channel-interacting protein

NCOA:

Nuclear receptor coactivator

NRIP:

Nuclear receptor interacting protein

PCs:

Principal components

Pn:

Pacemaker nucleus

SPPn:

Sublemniscal prepacemaker nucleus

SRC:

Steroid receptor coactivator

VMN:

Vocal motor nucleus

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Acknowledgements

The authors thank Jie Huang and James Ford at the Indiana University Center for Genomics and Bioinformatics for constructing and sequencing libraries, and the Indiana University Center for the Integrative Study of Animal Behavior (CISAB) Mechanisms of Behavior Core Laboratory for the use of facilities to isolate RNA from samples. Supported by NSF IOS 0950721 to GTS and NIH T32049336 to ARS. This research was supported in part by Lilly Endowment, Inc., through its support for the Indiana University Pervasive Technology Institute, and in part by the Indiana METACyt Initiative. The Indiana METACyt Initiative at IU was also supported in part by Lilly Endowment, Inc. Animal care and experimental procedures were in conducted in accordance with ethical standards in the NIH Guide and by using protocols approved by the Bloomington Institutional Animal Care and Use Committee at Indiana University.

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  1. Department of Biology, Indiana University, Jordan Hall, 1001 E. 3rd St., Bloomington, IN, 47405, USA

    G. Troy Smith, Melissa R. Proffitt, Adam R. Smith & Douglas B. Rusch

  2. Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, IN, 47405, USA

    G. Troy Smith, Melissa R. Proffitt & Adam R. Smith

  3. Center for Genomics and Bioinformatics, Indiana University, Bloomington, IN, 47405, USA

    Douglas B. Rusch

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  1. G. Troy Smith
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  2. Melissa R. Proffitt
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Correspondence to G. Troy Smith.

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Smith, G.T., Proffitt, M.R., Smith, A.R. et al. Genes linked to species diversity in a sexually dimorphic communication signal in electric fish. J Comp Physiol A 204, 93–112 (2018). https://doi.org/10.1007/s00359-017-1223-3

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  • DOI: https://doi.org/10.1007/s00359-017-1223-3

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