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

Lavoué S, Miya M, Arnegard ME, Sullivan JP, Hopkins CD, Nishida M - PLoS ONE (2012)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Oceanography, National Taiwan University, Taipei, Taiwan. microceb@hotmail.com

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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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).
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pone-0036287-g003: 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).

Mentions: Maximum likelihood (ML) analyses of the different data subsets yielded similar phylogenetic results, with topological differences only occurring for a few of the relationships (Fig. 3, S1, and S2). In all ML analyses across all three data subsets, the Gymnotiformes and the Mormyroidea are each monophyletic to the exclusion of all other teleosts (bootstrap proportion [BP]  = 100%). Moreover, these two clades of weakly electric fishes are nested within two distantly related groups of Teleostei, the Ostariophysi and the Osteoglossomorpha. Because the Osteoglossomorpha (with or without the Elopomorpha) is the most basal lineage in our tree, the most recent common ancestor of the Ostariophysi and the Osteoglossomorpha is also the most recent common ancestor of the crown-group Teleostei (Fig. 3).


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

Lavoué S, Miya M, Arnegard ME, Sullivan JP, Hopkins CD, Nishida M - PLoS ONE (2012)

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).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3351409&req=5

pone-0036287-g003: 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).
Mentions: Maximum likelihood (ML) analyses of the different data subsets yielded similar phylogenetic results, with topological differences only occurring for a few of the relationships (Fig. 3, S1, and S2). In all ML analyses across all three data subsets, the Gymnotiformes and the Mormyroidea are each monophyletic to the exclusion of all other teleosts (bootstrap proportion [BP]  = 100%). Moreover, these two clades of weakly electric fishes are nested within two distantly related groups of Teleostei, the Ostariophysi and the Osteoglossomorpha. Because the Osteoglossomorpha (with or without the Elopomorpha) is the most basal lineage in our tree, the most recent common ancestor of the Ostariophysi and the Osteoglossomorpha is also the most recent common ancestor of the crown-group Teleostei (Fig. 3).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Institute of Oceanography, National Taiwan University, Taipei, Taiwan. microceb@hotmail.com

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.

Show MeSH
Related in: MedlinePlus