Timing the rise of a weakly-electric sense

By Jesse Osborn (Scripps College) and Hillary Bruegl (Scripps College) [edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the Claremont Colleges]

The weakly electric sense of South American Gymnotiformes and the African Mormyridae is an amazing example of convergent evolution, i.e. the independent origin of similar biological traits from dissimilar ancestral states in unrelated lineages. This sense allows these fishes to not only receive electrical impulses, but also generate them. In a paper published in the journal PLoS One, Lavoue et al. examine the temporal pattern of the evolution of this fascinating sense organ in these two fish clades. Surprisingly, the timing of these separate origins is extremely similar (16-19 or 22-26 million years, depending on the calibration method) allowing for the investigation of pathways leading to evolutionarily novelty and influences of key innovations in communication on species radiation.

Electroreception is a widely distributed sense among non-teleost aquatic craniates. However among teleost fishes, it is restricted to two distantly related groups: the Gymnotiformes plus Siluriformes and the Mormyroidea plus Notopteridae. Gymnotiformes are freshwater naked-back knifefish that have an eel-like appearance. The only fin present is the anal fin, extending along most of the body. They are nocturnal and sometimes bury themselves in the substrate of deep rivers and swamps. Mormyroidea are freshwater elephantfishes and have fish-like form with an extended trunk-like mouth. The Gymnotiformes and Mormyroidea both evolved the ability to produce weak electric discharges used for electrolocation and communication in addition to having the high frequency electroreceptors that detect these discharges. The parallels between their electrical systems are extraordinary. First, they both evolved a novel myogenic electrical organ derived from skeletal muscle progenitor cells, as well as having the same sodium channel α-subunit gene duplicate. Second, the origin of high frequency electroreceptors is derived from similar lateral line precursors. Gymnotiformes and Mormyroidea also share other phenotypic similarities such as: body form, swimming behavior, reproductive behavior, nocturnal activity patterns, electric signal types, neural algorithms used to avoid jamming electrolocation and communication (Figure 1, below).

Morphological convergences between Mormyroidea and Gymnotiformes.

Figure 1. Morphological convergences between Mormyroidea and Gymnotiformes.

Prior to this study, no one had used a broad enough taxonomic sampling or a sufficiently large molecular data set to simultaneously and robustly estimate the ages of the origins of the electric organs in Gymnotiformes and Mormyroidea on a single tree. Lavoue et al. were able to provide comprehensive molecular evidence of phylogenetic independence but contemporaneous origins of Gymnotiformes and Mormyroidea. They saw similar amounts of time had elapsed between the origin of initial electroreception, as well as the subsequent origin of the electrogenesis organ. Additionally, they were able to place the evolution of these two groups in the temporal context of the earth and found that Gymnotiformes and Mormyroidea arose around the same time the South Atlantic Ocean formed but are unsure if their origins were before or after the complete separation of Africa and South America.

In order to derive a phylogenetic tree containing chronological origins of these electric senses, the authors used complete mitochondrial genomes as the character set. They used unique and extensive taxonomic sampling including several basal teleost species and 27 species of Mormyroidea and Gymnotiformes representing all families of weakly electric teleosts. They also used a relaxed-clock Bayesian method to infer phylogenetic relationships and divergence times simultaneously, and completed two reconstructions of the phylogeny: the first using strong maximum age constraints and the second using soft maximum age constraints.

Lavoue et al. found that the nodes representing the two independent origins of electrogenesis were supported under all data subsets and analyses. This finding was consistent with Arnegard et al’s phylogenetic hypothesis that was based off of a less complete mt-seq data set (2010). For the most part, phylogenetic relationships were also consistent with previously published hypothesis. A minor inconsistency was discovered in regards to Lavoue et al’s hypothesis that Isichthys, Brienomyrus and Mormyrus were a monophyletic group (2003). Instead they found that these three genera are sister groups of all Mormyroides. This new finding is important in creating the most accurate phylogeny and temporal scale for the evolution of this group and the electric senses.

Using these two reconstructions of the phylogeny, authors also found that the mean ages of Mormyroidea and Gymnotiformes are very similar to each other with less than a 15% difference. These origins were found to occur well after the split of the two lineages from their most recent common ancestor, between 185.7 Mya and 284.1 Mya using the two reconstructions. This finding was found to be congruent with previous paleontological evidence. Since this is such a large range, future studies could be used to narrow the range and provide more accurate timing.

Figure 2. Phylogenetic chronogram of the Teleostei using strong maximum age constraints.

Figure 2. Phylogenetic chronogram of the Teleostei using strong maximum age constraints.

Additionally, the independent origins of electrogenesis were found to occur roughly the same interval of time following the origins of electroreception (Gymnotiformes -100.2 Mya and Mormyroids-93.7 Mya). They also found that in both the Mormyroidea and Gymnotiformes, there was also a similar interval of time between the appearance of passive electroreception and the appearance of myogenic electric organ allowing for electrogenesis (Figure 2). These similar time intervals are the most interesting finding as they provide an empirically valuable case of convergent evolution, making this complete and temporally calibrated phylogeny extremely useful for evolutionary biologists studying the time period required for evolution to construct a weak myo-electric organ de novo from skeletal muscle precursors. The authors suspect that whole genome duplication occurred just prior to the radiation of teleosts contributed to the origin of novel electrogenesis in these two families.

Figure 3. The fracturing of Pangaea and the formation of the South Atlantic Ocean.

Figure 3. The fracturing of Pangaea and the formation of the South Atlantic Ocean.

Lastly, authors were able to use the temporal scale and fit the phylogeny to the paleogeographic history of the earth, allowing them to see that Gymnotiformes and Mormyroidea diverged around the same time as Gondwana, the southerly two supercontinents part of Pangaea, was almost completely fragmented apart (Figure 3). Although the divergence can’t be firmly placed as before or after the split, the authors speculate that the two shared environmental conditions during the early Late Cretaceous that may have contributed to their contemporaneous origins. Formally, the divergence has been placed near the beginning of the separation of the two continents.

Although this framework is as accurate as can be for the information given, future studies can always improve upon the accuracy of phylogenetic relationships and time calibration. The most important improvement could be made upon the exact time intervals between the independent origins of Mormyroidea and Gymnotiformes and the intervals between each family’s origins of electroreception and electrogenesis. This information can be used to further identify the evolutionary pathways used to form novel traits and locate these temporally. This study serves as an extraordinary and scientifically valuable case of convergent evolution in vertebrates.

References

Arnegard ME, Bogdanowicz SM, Hopkins CD. (2005). Multiple cases of striking genetic similarity between alternate electric fish signal morphs in sympatry. Evolution. 59: 324-343.

Lavoue S, Sullivan JP, Hopkins CD. (2003) Phylogenetic utility of the first two introns of the S7 ribosomal protein gene in African electric fishes (Mormyroidea: Teleostei) and congruence with other molecular markers. Biol J Linnean Soc. 78: 237-292.

Lavoue S, Miya M, Arnegard M, Sullivan JP, Hopkins CD, Nishida M. (2012). Comparable Ages for the Independent Origins of Electrogenesis in African and South American Weakly Electric Fishes. PLoS ONE. 7,5. 

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