Introduction
The gymnophionans (order Gymnophiona, class Amphibia), also known as caecilians, are limbless amphibians that generally live either in the soil or in water, and may superficially resemble earthworms or eels. About 180 living species are known, divided into 10 families. The phylogenetic context of the taxon is illustrated below:
The crown node of the gymnophionans is shown above as a black dot. In this section we will consider the evolution of the stem lines of the Gymnophiona and of the higher-order clade to which they belong, the amphibians. These stem lines are depicted as red and blue lines respectively in the above phylogenetic tree.
The stem group of the amphibians
The Amphibia, all of which lay their eggs in water, comprise two clades: the Gymnophiona and the Batrachia, which comprise the frogs, toads, newts and salamanders.
The phylogeny of the amphibian stem group is currently undergoing active research, and there are substantial areas of disagreement between different researchers. One interpretation, based on two fairly recent publications, is shown below:
The phylogeny of the amphibian stem group is currently undergoing active research, and there are substantial areas of disagreement between different researchers. One interpretation, based on two fairly recent publications, is shown below:
It is important to note that the above phylogenetic tree represents just one of three possible hypotheses for the origin of the amphibians. It is based on the Temnospondyl Hypothesis of Ruta and Coates (2007), whereby the modern amphibians evolved from dissorophoid temnospondyls. Alternative ideas are represented by the Lepospondyl Hypothesis (Laurin and Reisz, 1997), in which the amphibian crown group developed from the Lepospondyli, a group on the amniote stem, and the Polyphyletic Hypothesis, in which the modern amphibians are derived from separate groups of Paleozoic tetrapods (Sigurdsen and Green, 2011). Here we follow the Temnospondyl Hypothesis because it is favored by a majority of workers today. However, for an alternative view, see Marjanović and Laurin (2019).
The earliest known representative of the amphibian stem group is Balanerpeton woodi, found in the Early Carboniferous sediments in the East Kirkton Quarry, Bathgate, near Edinburgh, Scotland (Milner and Sequeira, 1993; Schoch, 2013). This species is illustrated, together with other fossil representatives of the stem group, in the following figure (for larger versions, click on images). The numbers in front of the names represent the order in which they appear in the above phylogenetic tree. The following series of images thus illustrates the transition from the most basal forms to species that are closest to the crown group.
The earliest known representative of the amphibian stem group is Balanerpeton woodi, found in the Early Carboniferous sediments in the East Kirkton Quarry, Bathgate, near Edinburgh, Scotland (Milner and Sequeira, 1993; Schoch, 2013). This species is illustrated, together with other fossil representatives of the stem group, in the following figure (for larger versions, click on images). The numbers in front of the names represent the order in which they appear in the above phylogenetic tree. The following series of images thus illustrates the transition from the most basal forms to species that are closest to the crown group.
* after name indicates that the image represents a life restoration.
To the casual observer there is no obvious consistent change through the series, except for a general shortening of tail length relative to total body length and the fact that some of the species closest to the crown group appear rather frog-like (e.g. Cacops, Amphibamus, Gerobatrachus). However, phylogenetic analysis (e.g. Schoch, 2019) has demonstrated important changes in skull morphology along the amphibian stem line.
The earliest known member of the crown-Amphibia is Triadobatrachus massinoti, a stem-group frog (i.e. crown-group batrachian) found in the Early Triassic (Late Induan - Early Olenekian) Sakamena Group of the Ambilobe district of the Diana Region, northwest Madagascar (Rage and Rocek, 1989; Sigurdsen et al, 2012). A fossil and a life restoration are shown below (click on image for a larger view):
The earliest known member of the crown-Amphibia is Triadobatrachus massinoti, a stem-group frog (i.e. crown-group batrachian) found in the Early Triassic (Late Induan - Early Olenekian) Sakamena Group of the Ambilobe district of the Diana Region, northwest Madagascar (Rage and Rocek, 1989; Sigurdsen et al, 2012). A fossil and a life restoration are shown below (click on image for a larger view):
The amphibian stem group evolved from Early Carboniferous to Early Triassic time, as illustrated in the following time tree:
This plot indicates that the stem-to-crown transition for the Amphibia lasted at least 80 million years. However, the ages of the known fossils suggest that most of the evolutionary change took place over a much shorter period of around 27 million years, during the Early Permian:
The stem group of the gymnophionans
The phylogeny of the stem-Gymphiona, based on the few known fossils, is illustrated below:
The oldest known member of the stem group is Chinlestegophis jenkinsi, from the Late Triassic (Middle - Late Norian) Chinle Formation at the Main Elk Creek locality, Garfield County, Colorado, USA (Pardo et al, 2017a). No public-domain images of this species are available, but the other two known stem gymnophionans are illustrated below (click on image for larger version):
* after name indicates that the image represents a life restoration.
With images of only two stem species it is not possible to discern any trend, but it is noteworthy that the two stem-group fossils restored above have small limbs, in contrast to the modern caecilians (however, no limbs were found for the fossil of Chinlestegophis jenkinsi, which comprises only a partial skull).
The earliest known fossil representative of crown-group Gymnophiona is Apodops pricei, found in a Late Paleocene fissure fill in the limestone quarry of the Companhia National de Cimento Portland, Rio de Janeiro, Brazil (Estes and Wake, 1972; Benton et al, 2015). Unfortunately, no images of this fossil are available in the public domain.
The gymnophionan stem group evolved from Late Triassic to Paleocene time, as illustrated in the following plot:
The earliest known fossil representative of crown-group Gymnophiona is Apodops pricei, found in a Late Paleocene fissure fill in the limestone quarry of the Companhia National de Cimento Portland, Rio de Janeiro, Brazil (Estes and Wake, 1972; Benton et al, 2015). Unfortunately, no images of this fossil are available in the public domain.
The gymnophionan stem group evolved from Late Triassic to Paleocene time, as illustrated in the following plot:
The above plot demonstrates that the stem-to-crown transition for the Gymnophiona lasted at least 147 million years. In fact, this is clearly an underestimate because of the ghost lineage representing the delay in appearance of the gymnophionans with respect to that of the Batrachia total group (note that no stem-group batrachians have yet been identified). Taking that into account, the stem-to-crown transition would have lasted at least 188 million years.
References
Benton, M. J., Donoghue, P. C., Asher, R. J., Friedman, M., Near, T. J., & Vinther, J. (2015). Constraints on the timescale of animal evolutionary history. Palaeontologia Electronica, 18(1), 1-106.
Estes, R., & WAKE, M. H. (1972). The first fossil record of caecilian amphibians. Nature, 239(5369), 228-231.
Laurin, M., Reisz, R. R., Sumida, S. S., & Martin, K. L. M. (1997). A new perspective on tetrapod phylogeny. Amniote origins: completing the transition to land, in Sumida S.S., and Martin, K.L., eds., Amniote Origins: New York, Academic Press, p. 9–59.
Marjanović, D., & Laurin, M. (2019). Phylogeny of Paleozoic limbed vertebrates reassessed through revision and expansion of the largest published relevant data matrix, PeerJ, 6, e5565.
Milner, A. R., & Sequeira, S. E. K. (1993). The temnospondyl amphibians from the Viséan of east Kirkton, West Lothian, Scotland. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 84(3-4), 331-361.
Pardo, J. D., Small, B. J., & Huttenlocker, A. K. (2017a). Stem caecilian from the Triassic of Colorado sheds light on the origins of Lissamphibia. Proceedings of the National Academy of Sciences, 114(27), E5389-E5395.
Rage, J. C., & Rocek, Z. (1989). Redescription of Triadobatrachus massinoti (Piveteau, 1936) an anuran amphibian from the early Triassic. Palaeontographica A, 206(1-3), 1-16.
Ruta, M., and Coates, M.I. (2007). Dates, nodes, and character conflict: addressing the lissamphian origin problem: Journal of Systematic Palaeontology, v. 5, p. 69–122.
Ruta, M., Krieger, J., Angielczyk, K. D., & Wills, M. A. (2018). The evolution of the tetrapod humerus: Morphometrics, disparity, and evolutionary rates. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 109(1-2), 351-369.
San Mauro, D., Gower, D. J., Müller, H., Loader, S. P., Zardoya, R., Nussbaum, R. A., & Wilkinson, M. (2014). Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Molecular phylogenetics and evolution, 73, 177-189.
Santos, R. O., Laurin, M., & Zaher, H. (2020). A review of the fossil record of caecilians (Lissamphibia: Gymnophionomorpha) with comments on its use to calibrate molecular timetrees. Biological Journal of the Linnean Society, 131(4), 737-755.
Schoch, R. R. (2013). The evolution of major temnospondyl clades: an inclusive phylogenetic analysis. Journal of Systematic Palaeontology, 11(6), 673-705.
Schoch, R. R. (2019). The putative lissamphibian stem-group: phylogeny and evolution of the dissorophoid temnospondyls. Journal of Paleontology, 93(1), p. 137–156. (doi: 10.1017/jpa.2018.67)
Sigurdsen, T., & Green, D. M. (2011). The origin of modern amphibians: a re-evaluation. Zoological Journal of the Linnean Society, 162(2), 457-469.
Sigurdsen, T., Green, D. M., & Bishop, P. J. (2012). Did Triadobatrachus jump? Morphology and evolution of the anuran forelimb in relation to locomotion in early salientians. Fieldiana Life and Earth Sciences, 77-89.
Estes, R., & WAKE, M. H. (1972). The first fossil record of caecilian amphibians. Nature, 239(5369), 228-231.
Laurin, M., Reisz, R. R., Sumida, S. S., & Martin, K. L. M. (1997). A new perspective on tetrapod phylogeny. Amniote origins: completing the transition to land, in Sumida S.S., and Martin, K.L., eds., Amniote Origins: New York, Academic Press, p. 9–59.
Marjanović, D., & Laurin, M. (2019). Phylogeny of Paleozoic limbed vertebrates reassessed through revision and expansion of the largest published relevant data matrix, PeerJ, 6, e5565.
Milner, A. R., & Sequeira, S. E. K. (1993). The temnospondyl amphibians from the Viséan of east Kirkton, West Lothian, Scotland. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 84(3-4), 331-361.
Pardo, J. D., Small, B. J., & Huttenlocker, A. K. (2017a). Stem caecilian from the Triassic of Colorado sheds light on the origins of Lissamphibia. Proceedings of the National Academy of Sciences, 114(27), E5389-E5395.
Rage, J. C., & Rocek, Z. (1989). Redescription of Triadobatrachus massinoti (Piveteau, 1936) an anuran amphibian from the early Triassic. Palaeontographica A, 206(1-3), 1-16.
Ruta, M., and Coates, M.I. (2007). Dates, nodes, and character conflict: addressing the lissamphian origin problem: Journal of Systematic Palaeontology, v. 5, p. 69–122.
Ruta, M., Krieger, J., Angielczyk, K. D., & Wills, M. A. (2018). The evolution of the tetrapod humerus: Morphometrics, disparity, and evolutionary rates. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 109(1-2), 351-369.
San Mauro, D., Gower, D. J., Müller, H., Loader, S. P., Zardoya, R., Nussbaum, R. A., & Wilkinson, M. (2014). Life-history evolution and mitogenomic phylogeny of caecilian amphibians. Molecular phylogenetics and evolution, 73, 177-189.
Santos, R. O., Laurin, M., & Zaher, H. (2020). A review of the fossil record of caecilians (Lissamphibia: Gymnophionomorpha) with comments on its use to calibrate molecular timetrees. Biological Journal of the Linnean Society, 131(4), 737-755.
Schoch, R. R. (2013). The evolution of major temnospondyl clades: an inclusive phylogenetic analysis. Journal of Systematic Palaeontology, 11(6), 673-705.
Schoch, R. R. (2019). The putative lissamphibian stem-group: phylogeny and evolution of the dissorophoid temnospondyls. Journal of Paleontology, 93(1), p. 137–156. (doi: 10.1017/jpa.2018.67)
Sigurdsen, T., & Green, D. M. (2011). The origin of modern amphibians: a re-evaluation. Zoological Journal of the Linnean Society, 162(2), 457-469.
Sigurdsen, T., Green, D. M., & Bishop, P. J. (2012). Did Triadobatrachus jump? Morphology and evolution of the anuran forelimb in relation to locomotion in early salientians. Fieldiana Life and Earth Sciences, 77-89.
Image credits - Gymnophiona
- Header (Microcaecilia dermatophaga): Wilkinson M, Sherratt E, Starace F, Gower DJ (2013) [CC BY 2.5 (https://creativecommons.org/licenses/by/2.5)], via Wikimedia Commons
- Edops craigi: Dmitry Bogdanov, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Skull of Cochleosaurus sp. (2a): Tommy from Arad, CC BY 2.0 <https://creativecommons.org/licenses/by/2.0>, via Wikimedia Commons
- Cochleosaurus sp. (2b): ДиБгд at Russian Wikipedia, Public domain, via Wikimedia Commons
- Eryops sp. (3a): Ed Bierman, CC BY 2.0 <https://creativecommons.org/licenses/by/2.0>, via Wikimedia Commons
- Eryops sp. (3b): Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Cheliderpeton latirostre (4a): Ghedoghedo, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Cheliderpeton vranyi (4b): Smokeybjb, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Archegosaurus sp. (5a): Daderot, CC0, via Wikimedia Commons
- Archegosaurus decheni (5b): Nobu Tamura, licensed under Creative Commons Attribution- ShareAlike (CC BY-SA)
- Australerpeton cosgriffi: Dmitry Bogdanov, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Balanerpeton woodi: Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Dendrerpeton acadianum (8a): Gary Todd, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Dendrerpeton sp. (8b): ДиБгд, Public domain, via Wikimedia Commons
- Skull of Trimerorhachis insignis (9a): Smokeybjb, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Trimerorhachis insignis (9b): Nobu Tamura, licensed under Creative Commons Attribution- ShareAlike (CC BY-SA)
- Acanthostomatops vorax: Dmitry Bogdanov, CC BY 3.0 <https://creativecommons.org/licenses/by/3.0>, via Wikimedia Commons
- Micromelerpeton credneri: Ghedoghedo, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Branchierpeton amblystomum: Dmitry Bogdanov, Attribution-NonCommercial-NoDerivs 3.0 Unported (CC BY-NC-ND 3.0)
- Skull of Conjunctio multidens: University of California Museum of Paleontology, Creative Commons Attribution 3.0 (CC BY 3.0) license
- Cacops sp. (14a): Jay Malone from Casselberry, FL, USA, CC BY 2.0 <https://creativecommons.org/licenses/by/2.0>, via Wikimedia Commons
- Cacops aspidephorus (14b): Nobu Tamura, licensed under Creative Commons Attribution- ShareAlike (CC BY-SA)
- Skull of Dissorophus multicinctus: University College London, Creative Commons, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Broiliellus olsoni: Smokeybjb, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Fedexia striegeli: Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Phonerpeton pricei: Smokeybjb, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Acheloma cumminsi (19a): Jonathan Chen, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Acheloma cumminsi (19b): ДиБгд, CC BY-SA 3.0 <http://creativecommons.org/licenses/by-sa/3.0/>, via Wikimedia Commons
- Eoscopus lockardi: Jeyradan, Public domain, via Wikimedia Commons
- Platyrhinops lyelli: Smokeybjb, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Micropholis stowi: Smokeybjb, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Amphibamus lyelli (23a): Experiencing Life Trips, Attribution-NonCommercial-ShareAlike 2.0 Generic (CC BY-NC-SA 2.0)
- Amphibamus grandiceps (23b): Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Apateon pedestris: Ghedoghedo, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Branchiosaurus salamandroides (25a): Ghedoghedo, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
- Branchiosaurus salamandroides (25b): Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Gerobatrachus hottoni (26a): Smithsonian Institution, Creative Commons Zero (CC0) license
- Gerobatrachus hottoni (26b): Nobu Tamura under a Creative Commons 3.0 Unported (CC BY-NC-ND 3.0) license
- Triadobatrachus massinoti (27a): Eduardo Ascarrunz; Jean-Claude Rage; Pierre Legreneur; Michel Laurin:, CC BY 3.0 <https://creativecommons.org/licenses/by/3.0>, via Wikimedia Commons
- Triadobatrachus massinoti (27b): Pavel.Riha.CB, CC BY-SA 3.0 <http://creativecommons.org/licenses/by-sa/3.0/>, via Wikimedia Commons
- Brain case of Eocaecilia macropodia (28a): Hillary C. Maddin, Farish A. Jenkins Jr, Jason S. Anderson [CC BY 2.5 (https://creativecommons.org/licenses/by/2.5)], via Wikimedia Commons
- Eocaecilia macropodia (28b): Nobu Tamura (http://spinops.blogspot.com) [GFDL (http://www.gnu.org/copyleft/fdl.html) or CC BY 3.0 (https://creativecommons.org/licenses/by/3.0)], from Wikimedia Commons
- Jawbone of Rubricacaecilia monbaroni (29a): Roberto Díaz Sibaja, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
- Rubricacaecilia monbaroni (29b): Levi Bernardo Martínez [CC0], from Wikimedia Commons