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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 distribution of electroreception within the Craniata and its evolution according to the criterion of parsimony.The phylogenetic backbone shown here follows Nelson [140], with modifications according to Gardiner et al. [141], Lavoué et al. [119], [142], Heimberg et al. [143], Kikugawa et al. [144], Li et al. [120], and Takezaki et al. [145]. Approximate timeline adapted from the fossil record; data on electroreception and electroreceptors taken from Bullock et al. [1], [26] and Albert and Crampton [25]. 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 [146]. Recently, Czech-Damal et al. [147] 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 [140]; other tetrapod illustrations taken from Léo Lavoué’s coloring book.
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pone-0036287-g001: Phylogenetic distribution of electroreception within the Craniata and its evolution according to the criterion of parsimony.The phylogenetic backbone shown here follows Nelson [140], with modifications according to Gardiner et al. [141], Lavoué et al. [119], [142], Heimberg et al. [143], Kikugawa et al. [144], Li et al. [120], and Takezaki et al. [145]. Approximate timeline adapted from the fossil record; data on electroreception and electroreceptors taken from Bullock et al. [1], [26] and Albert and Crampton [25]. 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 [146]. Recently, Czech-Damal et al. [147] 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 [140]; other tetrapod illustrations taken from Léo Lavoué’s coloring book.

Mentions: Electroreception, the ability to sense weak electric fields, is widely distributed in non-teleost aquatic craniates (Fig. 1). Ampullary electroreceptors, which are tuned to passively produced, low frequency electric fields, are found in lineages ranging from jawless craniates (lampreys) to several groups of “ancient fishes” such as chondrichthyans, coelacanths, and sturgeons [1], [25], [26]. This pattern suggests that electroreception is an ancient sense within the Craniata. However, because several hypotheses concerning reconstruction of the evolution of electroreception are equally parsimonious, it cannot be determined whether the most recent common ancestor of all craniates was electroreceptive (Fig. 1). Within teleost fishes–by far the largest group of vertebrates with more than 31,000 species [27]–electroreception is restricted to only two distantly related groups: the Siluriphysi sensu Fink and Fink [28] (i.e., the Gymnotiformes plus Siluriformes) and the Notopteroidei (i.e., the Mormyroidea plus Notopteridae). The most parsimonious hypothesis for this peculiar pattern is that low frequency electroreception was lost in the most recent common ancestor of the Neopterygii, only to be independently re-acquired in the Siluriphysi and the Notopteroidei (Fig. 1). Whereas the African Notopteridae and Siluriformes are only passively electroreceptive, the Gymnotiformes and the Mormyroidea secondarily and independently evolved specialized electric organs dedicated to the production of weak electric discharges, in addition to high-frequency (tuberous) electroreceptors that are tuned to these signals. Together, their electric organs and tuberous electroreceptors mediate both electrical communication and “active electrolocation” (e.g. [29]), in which objects are located in space and their electrical properties sensed via distortions in the self-generated electric field [30]. Thus, the ability to first sense low frequency, passive electric fields appears to have preceded the evolution of electrogenesis in the Gymnotiformes and Mormyroidea [31], [32].


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 distribution of electroreception within the Craniata and its evolution according to the criterion of parsimony.The phylogenetic backbone shown here follows Nelson [140], with modifications according to Gardiner et al. [141], Lavoué et al. [119], [142], Heimberg et al. [143], Kikugawa et al. [144], Li et al. [120], and Takezaki et al. [145]. Approximate timeline adapted from the fossil record; data on electroreception and electroreceptors taken from Bullock et al. [1], [26] and Albert and Crampton [25]. 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 [146]. Recently, Czech-Damal et al. [147] 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 [140]; other tetrapod illustrations taken from Léo Lavoué’s coloring book.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0036287-g001: Phylogenetic distribution of electroreception within the Craniata and its evolution according to the criterion of parsimony.The phylogenetic backbone shown here follows Nelson [140], with modifications according to Gardiner et al. [141], Lavoué et al. [119], [142], Heimberg et al. [143], Kikugawa et al. [144], Li et al. [120], and Takezaki et al. [145]. Approximate timeline adapted from the fossil record; data on electroreception and electroreceptors taken from Bullock et al. [1], [26] and Albert and Crampton [25]. 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 [146]. Recently, Czech-Damal et al. [147] 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 [140]; other tetrapod illustrations taken from Léo Lavoué’s coloring book.
Mentions: Electroreception, the ability to sense weak electric fields, is widely distributed in non-teleost aquatic craniates (Fig. 1). Ampullary electroreceptors, which are tuned to passively produced, low frequency electric fields, are found in lineages ranging from jawless craniates (lampreys) to several groups of “ancient fishes” such as chondrichthyans, coelacanths, and sturgeons [1], [25], [26]. This pattern suggests that electroreception is an ancient sense within the Craniata. However, because several hypotheses concerning reconstruction of the evolution of electroreception are equally parsimonious, it cannot be determined whether the most recent common ancestor of all craniates was electroreceptive (Fig. 1). Within teleost fishes–by far the largest group of vertebrates with more than 31,000 species [27]–electroreception is restricted to only two distantly related groups: the Siluriphysi sensu Fink and Fink [28] (i.e., the Gymnotiformes plus Siluriformes) and the Notopteroidei (i.e., the Mormyroidea plus Notopteridae). The most parsimonious hypothesis for this peculiar pattern is that low frequency electroreception was lost in the most recent common ancestor of the Neopterygii, only to be independently re-acquired in the Siluriphysi and the Notopteroidei (Fig. 1). Whereas the African Notopteridae and Siluriformes are only passively electroreceptive, the Gymnotiformes and the Mormyroidea secondarily and independently evolved specialized electric organs dedicated to the production of weak electric discharges, in addition to high-frequency (tuberous) electroreceptors that are tuned to these signals. Together, their electric organs and tuberous electroreceptors mediate both electrical communication and “active electrolocation” (e.g. [29]), in which objects are located in space and their electrical properties sensed via distortions in the self-generated electric field [30]. Thus, the ability to first sense low frequency, passive electric fields appears to have preceded the evolution of electrogenesis in the Gymnotiformes and Mormyroidea [31], [32].

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