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Comparative Study
. 2012;7(5):e36287.
doi: 10.1371/journal.pone.0036287. Epub 2012 May 14.

Comparable ages for the independent origins of electrogenesis in African and South American weakly electric fishes

Sébastien Lavoué  1 , Masaki Miya, Matthew E Arnegard, John P Sullivan, Carl D Hopkins, Mutsumi Nishida
Affiliations
Comparative Study

Comparable ages for the independent origins of electrogenesis in African and South American weakly electric fishes

Sébastien Lavoué et al. PLoS One. 2012.

Abstract

One of the most remarkable examples of convergent evolution among vertebrates is illustrated by the independent origins of an active electric sense in South American and African weakly electric fishes, the Gymnotiformes and Mormyroidea, respectively. These groups independently evolved similar complex systems for object localization and communication via the generation and reception of weak electric fields. While good estimates of divergence times are critical to understanding the temporal context for the evolution and diversification of these two groups, their respective ages have been difficult to estimate due to the absence of an informative fossil record, use of strict molecular clock models in previous studies, and/or incomplete taxonomic sampling. Here, we examine the timing of the origins of the Gymnotiformes and the Mormyroidea using complete mitogenome sequences and a parametric bayesian method for divergence time reconstruction. Under two different fossil-based calibration methods, we estimated similar ages for the independent origins of the Mormyroidea and Gymnotiformes. Our absolute estimates for the origins of these groups either slightly postdate, or just predate, the final separation of Africa and South America by continental drift. The most recent common ancestor of the Mormyroidea and Gymnotiformes was found to be a non-electrogenic basal teleost living more than 85 millions years earlier. For both electric fish lineages, we also estimated similar intervals (16-19 or 22-26 million years, depending on calibration method) between the appearance of electroreception and the origin of myogenic electric organs, providing rough upper estimates for the time periods during which these complex electric organs evolved de novo from skeletal muscle precursors. The fact that the Gymnotiformes and Mormyroidea are of similar age enhances the comparative value of the weakly electric fish system for investigating pathways to evolutionary novelty, as well as the influences of key innovations in communication on the process of species radiation.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Phylogenetic distribution of electroreception within the Craniata and its evolution according to the criterion of parsimony.
The phylogenetic backbone shown here follows Nelson , with modifications according to Gardiner et al. , Lavoué et al. , , Heimberg et al. , Kikugawa et al. , Li et al. , and Takezaki et al. . Approximate timeline adapted from the fossil record; data on electroreception and electroreceptors taken from Bullock et al. , and Albert and Crampton . Colored branches indicate electroreceptive lineages possessing electroreceptors: as modified mucous glands (orange); of the ampullary sense organ type (deep blue); of both the tuberous sense organ type and the ampullary sense organ type found in teleosts (yellow). White branches signify non-electroreceptive lineages following secondary loss of electroreceptive capability; four (possibly five) such losses are indicated by white hash marks. The origins of different forms of electroreception are indicated by black hash marks. The electroreceptive conditions of the ancestors of the Craniata and of the clade (hagfishes, lampreys) are unresolved (indicated with grey and question marks) because there are several equi-parsimonious hypotheses concerning them. The end bud electroreceptor of the lampreys and the ampullary electroreceptor of the basal gnathostomes are anatomically very different, suggesting independent origins. The tree does not map atypical reports of electroreceptive gains in single species, which are in need of further study, such as tuberous electroreceptors in a blind catfish . Recently, Czech-Damal et al. discovered a novel sensory organ and possible electroreceptors associated with the hairless vibrissal crypts on the snout of the Guiana Dolphin (Sotalia guianensis), which appear to be sensitive to weak D.C. electric fields on the order of 4.6 microvolts per cm. Although their studies so far involve only one captive specimen trained to respond to the presence or absence of weak electric fields, it indeed suggests that additional research is needed on the sensory capabilities of aquatic mammals that might have independently evolved electroreception. Piranha (Catoprion mento) and platypus illustrations modified from images downloaded from Wikimedia Commons; paddlefish (Polyodon spathula) illustration modified from NOAA’s Historic Fisheries Collection Catalog of Images; other fish illustrations modified from Nelson ; other tetrapod illustrations taken from Léo Lavoué’s coloring book.
Figure 2
Figure 2. Morphological convergences between African and South American electric fishes.
Mormyroid African electric fishes (left column) are facing gymnotiform South American electric fishes (right column) with similar aspects of morphology (such as elongate bodies, extended tube-like snouts, reduced eyes, and/or small mouth sizes). Anterior portion of body shown above small image of whole body (except for Petrocephalus sullivani); electric organ discharge waveform shown for every species (each trace 5 ms in total duration with head-positivity plotted upwards). (A) Mormyrops zanclirostris, 175 mm standard length (SL), Ivindo River, Gabon, (B) Sternarchorhynchus oxyrhynchus, 220 mm total length (TL), Rio Negro, Brazil; (C) Mormyrus proboscirostris, 232 mm standard length, Ubundu, Congo River, D.R. Congo; (D) Rhamphichthys sp., 305 mm TL, Rio Negro, Brazil; (E) Mormyrops anguilloides, 195 mm SL, Yangambi, Congo River, D.R. Congo; (F) Gymnotus sp., 195 mm TL, Rio Negro, Brazil; and (G) Petrocephalus sullivani, Ogooué River, Gabon; (H) Eigenmannia sp., Apure River, Venezuela. Species A–D feed on benthic invertebrates, species E, F are piscivorous, and G, H feed on pelagic invertebrates.
Figure 3
Figure 3. Best maximum likelihood tree of the Teleostei from analysis of the mt-seq data subset “12RT,” using the software RAxML.
Branch lengths are proportional to the number of substitutions per nucleotide position (scale bar  = 0.05 substitutions). Numbers at nodes give node support in terms of bootstrap proportions. The tree is rooted with Amia calva. Light grey gradient boxes highlight the Mormyroidea (African weakly electric fishes) and the Gymnotiformes (South American weakly electric fishes). Arrowheads indicate nodes for which topological differences were found compared to trees reconstructed using the two other data subsets (“123ryRT” and “123RT,” shown in Fig. S1 and S2, respectively).
Figure 4
Figure 4. Phylogenetic chronogram of the Teleostei based on a Bayesian relaxed clock approach using the mt-seq data subset “12RT” under the first fossil calibration strategy.
In this approach, we used seven fossil-derived calibration constraints following lognormal distributions and ten others following uniform distributions (i.e., reconstruction #1). Amia calva is used to root the tree. Light grey gradient boxes highlight the Mormyroidea and Gymnotiformes. Horizontal timescale is in millions of years ago (Mya). Only selected epoch names are given. Abbreviations: E, early; Paleo, Paleocene; Eo, Eocene; and Oligo, Oligocene. Standardized timescale colors taken from the Commission for the Geological Map of the World. 95% age credibility intervals are shown as black and grey horizontal bars (calibration constraints on corresponding nodes), yellow horizontal bars (focal nodes of interest), and white horizontal bars (all other nodes). Daggers indicate that minimum ages were used to calibrate the nodes, and adjacent numbers in brackets refer to source fossils listed in the Materials and Methods. Numbers at nodes are the posterior probability support values (shown only when <1). Timing of the separation of Africa and South America is depicted by the three insets at the top, modified from . Here, “origin of electroreception” refers to the initial origin of any kind of electroreceptive system in the broadest sense (see text for elaboration).
Figure 5
Figure 5. Phylogenetic chronogram of the Teleostei based on a Bayesian relaxed clock approach using the mt-seq data subset “12RT” under the second fossil calibration strategy.
In this approach, we used 17 fossil-derived calibration constraints following uniform distributions (i.e., reconstruction #2). 95% age credibility intervals are shown as black horizontal bars (calibration constraints on corresponding nodes), yellow horizontal bars (focal nodes of interest), and white horizontal bars (all other nodes). Daggers indicate that minimum ages were used to calibrate the nodes, and adjacent numbers in brackets refer to source fossils listed in the Materials and Methods. Dashed lines between daggers and lower age limits of corresponding nodes (within the 95% age credibility intervals) depict putative ghost lineages in the fossil record. All other details as in Fig. 4.
Figure 6
Figure 6. Distributions of estimated ages for focal nodes of interest under each fossil calibration scheme.
For each plot, estimated ages were sampled every 5,000 generations from two independent BEAST runs of 1×108 generations each. Resulting age histograms are shown for the estimated times of the most recent common ancestors (tMRCAs) of the Mormyroidea and the Gymnotiformes (A) under reconstruction #1 (also see Fig. 4) and (C) under reconstruction #2 (also see Fig. 5); histograms are similarly shown for tMRCAs of the Notopteroidei and the Characiphysae under (B) reconstruction #1 and (D) reconstruction #2. The span of blue bars along the vertical axis of each plot gives the 95% credibility interval for that particular age estimate. Tails of each distribution are shown in red. All time scales in millions of years ago (Mya).
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