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Signal variation and its morphological correlates in Paramormyrops kingsleyae provide insight into the evolution of electrogenic signal diversity in mormyrid electric fish

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Abstract

We describe patterns of geographic variation in electric signal waveforms among populations of the mormyrid electric fish species Paramormyrops kingsleyae. This analysis includes study of electric organs and electric organ discharge (EOD) signals from 553 specimens collected from 12 localities in Gabon, West-Central Africa from 1998 to 2009. We measured time, slope, and voltage values from nine defined EOD “landmarks” and determined peak spectral frequencies from each waveform; these data were subjected to principal components analysis. The majority of variation in EODs is explained by two factors: the first related to EOD duration, the second related to the magnitude of the weak head-negative pre-potential, P0. Both factors varied clinally across Gabon. EODs are shorter in eastern Gabon and longer in western Gabon. Peak P0 is slightly larger in northern Gabon and smaller in southern Gabon. P0 in the EOD is due to the presence of penetrating-stalked (Pa) electrocytes in the electric organ while absence is due to the presence of non-penetrating stalked electrocytes (NPp). Across Gabon, the majority of P. kingsleyae populations surveyed have only individuals with P0-present EODs and Pa electrocytes. We discovered two geographically distinct populations, isolated from others by barriers to migration, where all individuals have P0-absent EODs with NPp electrocytes. At two sites along a boundary between P0-absent and P0-present populations, P0-absent and P0-present individuals were found in sympatry; specimens collected there had electric organs of intermediate morphology. This pattern of geographic variation in EODs is considered in the context of current phylogenetic work. Multiple independent paedomorphic losses of penetrating stalked electrocytes have occurred within five Paramormyrops species and seven genera of mormyrids. We suggest that this key anatomical feature in EOD signal evolution may be under a simple mechanism of genetic control, and may be easily influenced by selection or drift throughout the evolutionary history of mormyrids.

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Notes

  1. P. kingsleyae has been previously referred to using several operational taxonomic designators. Brienomyrus brachyistius (Long Biphasic or LBP) was used originally by Hopkins (1980), Hopkins and Bass (1981), Bass (1986a, b, c), Bass et al. (1986) and Hopkins (1986). As different regions of Gabon were explored, newly discovered allopatric populations were called Brienomyrus BN1, Brienomyrus BP1, Brienomyrus BX1, Brienomyrus LIB, Brienomyrus CAB by Sullivan et al. (2002), Arnegard and Hopkins (2003), Sullivan et al. (2004) and Arnegard et al. (2005). Eventually, all of the above populations were recognized as a single species P. kingsleyae, on the basis of genetic similarity, similar morphology and ecology, and overall EOD similarity. The most current diagnosis of Paramormyrops (formerly “the Gabon-Clade Brienomyrus”) and P. kingsleyae is summarized by Hopkins et al. (2007), and is provided for convenience as Online Resource 1.

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Acknowledgments

Permits to collect fishes in Gabon and export them for this study were granted by l’Institut de Recherche en Ecologie Tropicale, l’Institut de Recherches Agronomiques et Forestières and the Centre National de la Recherche Scientifique et Technologique. We are grateful for the valuable assistance and logistical support we received from J. D. Mbega and students working in these institutions. All techniques used are in accordance with protocols approved by Cornell University’s Center for Research Animal Resources and Education (CARE). The authors thank G. Harned for assistance with histological processing, Charles Dardia at the Cornell Museum of Vertebrates for assistance in the preparation of Online Resource 2, Cornell Microscopy and Imaging Core Facility for use of their confocal microscopy equipment. Additionally, we thank A. McCune and K. Shaw, as well as two anonymous reviewers for comments on earlier versions of this manuscript. This work was supported by NIMH TG T32 MH015793 and NIH TG 2T32GM007469 to JRG, NIH RO1-DC6206 and NSF 0818305 to CDH, and NSF 0818390 to BAC.

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Authors and Affiliations

  1. Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, USA

    Jason R. Gallant & Carl D. Hopkins

  2. Department of Zoology, University of British Columbia, Vancouver, Canada

    Matthew E. Arnegard

  3. Museum of Vertebrates, Cornell University, Ithaca, NY, USA

    John P. Sullivan

  4. Department of Biology, Washington University in St. Louis, St. Louis, MO, USA

    Bruce A. Carlson

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  1. Jason R. Gallant
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  2. Matthew E. Arnegard
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  4. Bruce A. Carlson
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  5. Carl D. Hopkins
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Correspondence to Jason R. Gallant.

Electronic supplementary material

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359_2011_643_MOESM1_ESM.pdf

Online Resource 1 For the convenience of the reader, the most recent diagnosis of Paramormyrops and P. kingsleyae is provided. Full text is available from: Hopkins CD, Lavoué S, Sullivan JP (2007) Mormyridae. In: Stiassny MLJ, Teugels GG, Hopkins CD (eds) Poissons D’eaux Douces Et Saumâtres De Basse Guinée: ouest de l’Afrique Central vol 1. Faune Et Flore Tropicales. IRD Éditions, Paris, pp 220–334. (PDF 145 kb)

359_2011_643_MOESM2_ESM.pdf

Online Resource 2 Tabulated list of all specimens included in this study. Their date of collection, collection coordinates, assigned locality, standard length (SL), sex, Cornell University Museum of Vertebrates accession numbers, and individual voucher numbers are included. (-) indicates no data available for sex and (ND) indicates no data available for standard length. (PDF 185 kb)

359_2011_643_MOESM3_ESM.pdf

Online Resource 3 Detailed discussion of temperature correction and its effects on EOD variation; variation due to temperature differences are compared to between and within population variation. (PDF 1364 kb)

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Gallant, J.R., Arnegard, M.E., Sullivan, J.P. et al. Signal variation and its morphological correlates in Paramormyrops kingsleyae provide insight into the evolution of electrogenic signal diversity in mormyrid electric fish. J Comp Physiol A 197, 799–817 (2011). https://doi.org/10.1007/s00359-011-0643-8

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