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

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.

Genetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fishParamormyrops kingsleyae

“…To better understand how broad macroevolutionary patterns in EOD trait divergence resulted from processes acting among individual populations, Gallant et al (2011) examined patterns of geographic variation among the highly vagile, geographically widespread Paramormyrops species, P. kingsleyae. P. kingsleyae exhibit clinal variation in EOD signals with regard to duration, and are polymorphic with regard to a small head-negative phase, termed P0 (Fig.…”

“…This hypothesis is based on several lines of evidence. First, Gallant et al (2011) ruled out several adaptive explanations for intraspecific EOD diversity within P. kingsleyae given the small magnitude of phase P0, together with lack of correlated variation in EOD waveform with environmental variables, predators or sympatric species. Second, a previous study provided evidence of substantial genetic partitioning between two allopatric populations of P. kingsleyae in southern Gabon (Arnegard et al, 2005), motivating the hypothesis that genetic drift between geographically isolated populations sufficiently explained the pattern of EOD signal variation among P. kingsleyae.…”

“…Second, a previous study provided evidence of substantial genetic partitioning between two allopatric populations of P. kingsleyae in southern Gabon (Arnegard et al, 2005), motivating the hypothesis that genetic drift between geographically isolated populations sufficiently explained the pattern of EOD signal variation among P. kingsleyae. Third, Gallant et al (2011) To test the overall hypothesis that genetic drift is sufficient to explain patterns of EOD diversity between geographically isolated populations of P. kingsleyae, we examined variation in population genetic structure using microsatellite genotyping within and between P. kingsleyae populations with divergent EOD signal types across Gabon, and found that EOD variation is highly correlated with patterns of genetic variation between populations. In the second experiment, we assessed the ability of field-captured and laboratory maintained P. kingsleyae to discriminate divergent P. kingsleyae EOD waveforms.…”

“…Mormyrids communicate using electric signals termed electric organ discharges (EODs). These signals are highly diverse and are easily measured and quantified; importantly, they have a well-characterized and discrete anatomical and physiological basis related to the function of other electrically excitable tissues such as muscle and nerve (Bennett and Grundfest 1961;Arnegard et al 2010a;Gallant et al 2011;Carlson and Gallant 2013). The electric modality, when compared to other signaling modalities, is relatively free from constraint: electric signals travel at the speed of light without distortion from the environment (Hopkins 1999), and by virtue of few other sympatric electroreceptive organisms are relatively private from eavesdropping by predators (Stoddard 1999).…”

Sexual selection by female choice prevents speciation reversal in a hybridizing trio of mormyrid fish in southern Africa: evidence from playback experiments of electric organ discharges

“…However, these species pairings using commercially acquired specimens did not include closest relatives and, therefore, the question of whether or not differentiation of IDI patterns was driving speciation remained unresolved. Other studies examining speciation in close mormyrid relatives include those of Arnegard et al (2005) (focussing on EOD waveform polymorphism in Brienomyrus species) and Arnegard et al (2006Arnegard et al ( , 2010 and Gallant et al (2011), the latter focussing on electric organ morphology. Arnegard et al (2006) focussed EOD features coded by knollenorgan electroreceptor organs, and Arnegard et al (2010) on ecological divergence.…”