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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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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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pone-0036287-g006: 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).

Mentions: With each reconstruction method, the mean ages of the Mormyroidea and the Gymnotiformes were found to be very similar to each other (<15% difference under both calibration strategies), with largely overlapping credibility intervals (Fig. 6). The mean ages of the Notopteroidei and Characiphysae were also quite similar between methods, with the Characiphysae slightly older than the Notopteroidei (Fig. 6). Nodes defining the latter two clades also define minimum age estimates for the independent origins of electroreception among teleosts (i.e., in the form of derived ampullary electroreceptors; see Fig. 1). Strikingly, the intervals between these estimates for the early origins of teleost electroreception, in this broadest sense of any form of electroreception, and the corresponding estimates for the origins of electrogenesis are quite similar for the two lineages of weakly electric fishes: the mean estimated interval is 16.6 My for mormyroids vs. 18.7 My for gymnotiforms under reconstruction #1, and 22.7 My vs. 25.6 My under reconstruction #2). Thus, the independent origins of electrogenesis may have occurred after roughly the same intervals of time following the independent origins of teleost electroreception in the broad sense. However, these nodes define only minimum ages for the origin of electroreception and electrogenesis, respectively. Each trait actually evolved somewhere along the stems that subtend those nodes, and we cannot estimate the actual origin of these novel innovations with any greater precision.


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)

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).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0036287-g006: 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).
Mentions: With each reconstruction method, the mean ages of the Mormyroidea and the Gymnotiformes were found to be very similar to each other (<15% difference under both calibration strategies), with largely overlapping credibility intervals (Fig. 6). The mean ages of the Notopteroidei and Characiphysae were also quite similar between methods, with the Characiphysae slightly older than the Notopteroidei (Fig. 6). Nodes defining the latter two clades also define minimum age estimates for the independent origins of electroreception among teleosts (i.e., in the form of derived ampullary electroreceptors; see Fig. 1). Strikingly, the intervals between these estimates for the early origins of teleost electroreception, in this broadest sense of any form of electroreception, and the corresponding estimates for the origins of electrogenesis are quite similar for the two lineages of weakly electric fishes: the mean estimated interval is 16.6 My for mormyroids vs. 18.7 My for gymnotiforms under reconstruction #1, and 22.7 My vs. 25.6 My under reconstruction #2). Thus, the independent origins of electrogenesis may have occurred after roughly the same intervals of time following the independent origins of teleost electroreception in the broad sense. However, these nodes define only minimum ages for the origin of electroreception and electrogenesis, respectively. Each trait actually evolved somewhere along the stems that subtend those nodes, and we cannot estimate the actual origin of these novel innovations with any greater precision.

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