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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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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.
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pone-0036287-g005: 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.

Mentions: The two methods used to calibrate our chronogram produced different age estimates for the independent origins of weakly electric teleost fishes, as well as for deeper nodes in the tree (Fig. 4 and 5). Using reconstruction #1 (with strong maximum age constraints, Fig. 4), the age of the crown-group Notopteroidei and the age of the crown-group Mormyroidea were estimated to be 110.3 Mya (95% credibility interval [CI]  = 91.7–127.2 Mya) and 93.7 Mya (CI  = 74.3–112.9 Mya), respectively. The age of the most recent common ancestor of the clade (Gymnotiformes, (Siluriformes, Characiformes)), named the Characiphysae by Wiley and Johnson [92], was estimated to be 118.9 Mya (CI  = 107.6–130.1 Mya), and the age of the crown-group Gymnotiformes was estimated to be 100.2 Mya (CI  = 84.9–115.3 Mya). The second method of reconstruction (#2, with only soft maximum age constraints, Fig. 5) yielded uniformly older age estimates for the entire tree, with the ages of the Notopteroidei, the crown-group Mormyroidea, the Characiphysae, and the crown-group Gymnotiformes estimated to 147.5 Mya (CI  = 117.9–177.9 Mya), 124.8 Mya (CI  = 97.5–155.7 Mya), 169.1 Mya (CI  = 140.5–197.3 Mya), and 143.5 Mya (CI  = 115.8–171.8 Mya), respectively.


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)

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.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0036287-g005: 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.
Mentions: The two methods used to calibrate our chronogram produced different age estimates for the independent origins of weakly electric teleost fishes, as well as for deeper nodes in the tree (Fig. 4 and 5). Using reconstruction #1 (with strong maximum age constraints, Fig. 4), the age of the crown-group Notopteroidei and the age of the crown-group Mormyroidea were estimated to be 110.3 Mya (95% credibility interval [CI]  = 91.7–127.2 Mya) and 93.7 Mya (CI  = 74.3–112.9 Mya), respectively. The age of the most recent common ancestor of the clade (Gymnotiformes, (Siluriformes, Characiformes)), named the Characiphysae by Wiley and Johnson [92], was estimated to be 118.9 Mya (CI  = 107.6–130.1 Mya), and the age of the crown-group Gymnotiformes was estimated to be 100.2 Mya (CI  = 84.9–115.3 Mya). The second method of reconstruction (#2, with only soft maximum age constraints, Fig. 5) yielded uniformly older age estimates for the entire tree, with the ages of the Notopteroidei, the crown-group Mormyroidea, the Characiphysae, and the crown-group Gymnotiformes estimated to 147.5 Mya (CI  = 117.9–177.9 Mya), 124.8 Mya (CI  = 97.5–155.7 Mya), 169.1 Mya (CI  = 140.5–197.3 Mya), and 143.5 Mya (CI  = 115.8–171.8 Mya), respectively.

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