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15.3: Clades of Amphibians - Biology

15.3: Clades of Amphibians - Biology


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Amphibia comprises an estimated 6,770 extant species that inhabit tropical and temperate regions around the world. Amphibians can be divided into three clades: Urodela (“tailed-ones”), the salamanders; Anura (“tail-less ones”), the frogs; and Apoda (“legless ones”), the caecilians.

Urodela: Salamanders

Salamanders are amphibians that belong to the order Urodela. Living salamanders (Figure 1) include approximately 620 species, some of which are aquatic, other terrestrial, and some that live on land only as adults. Adult salamanders usually have a generalized tetrapod body plan with four limbs and a tail. They move by bending their bodies from side to side, called lateral undulation, in a fish-like manner while “walking” their arms and legs fore and aft. It is thought that their gait is similar to that used by early tetrapods. Respiration differs among different species. The majority of salamanders are lungless, and respiration occurs through the skin or through external gills. Some terrestrial salamanders have primitive lungs; a few species have both gills and lungs.

Unlike frogs, virtually all salamanders rely on internal fertilization of the eggs. The only male amphibians that possess copulatory structures are the caecilians, so fertilization among salamanders typically involves an elaborate and often prolonged courtship. Such a courtship allows the successful transfer of sperm from male to female via a spermatophore. Development in many of the most highly evolved salamanders, which are fully terrestrial, occurs during a prolonged egg stage, with the eggs guarded by the mother. During this time, the gilled larval stage is found only within the egg capsule, with the gills being resorbed, and metamorphosis being completed, before hatching. Hatchlings thus resemble tiny adults.

View River Monsters: Fish With Arms and Hands? to see a video about an unusually large salamander species.

Anura: Frogs

Frogs are amphibians that belong to the order Anura (Figure 2a). Anurans are among the most diverse groups of vertebrates, with approximately 5,965 species that occur on all of the continents except Antarctica. Anurans have a body plan that is more specialized for movement. Adult frogs use their hind limbs to jump on land. Frogs have a number of modifications that allow them to avoid predators, including skin that acts as camouflage. Many species of frogs and salamanders also release defensive chemicals from glands in the skin that are poisonous to predators.

Frog eggs are fertilized externally, and like other amphibians, frogs generally lay their eggs in moist environments. A moist environment is required as eggs lack a shell and thus dehydrate quickly in dry environments. Frogs demonstrate a great diversity of parental behaviors, with some species laying many eggs and exhibiting little parental care, to species that carry eggs and tadpoles on their hind legs or backs. The life cycle of frogs, as other amphibians, consists of two distinct stages: the larval stage followed by metamorphosis to an adult stage. The larval stage of a frog, the tadpole, is often a filter-feeding herbivore. Tadpoles usually have gills, a lateral line system, long-finned tails, and lack limbs. At the end of the tadpole stage, frogs undergo metamorphosis into the adult form (Figure 2b). During this stage, the gills, tail, and lateral line system disappear, and four limbs develop. The jaws become larger and are suited for carnivorous feeding, and the digestive system transforms into the typical short gut of a predator. An eardrum and air-breathing lungs also develop. These changes during metamorphosis allow the larvae to move onto land in the adult stage.

Apoda: Caecilians

An estimated 185 species comprise caecilians (Figure 3), a group of amphibians that belong to the order Apoda. Although they are vertebrates, a complete lack of limbs leads to their resemblance to earthworms in appearance.

They are adapted for a soil-burrowing or aquatic lifestyle, and they are nearly blind. These animals are found in the tropics of South America, Africa, and Southern Asia. They have vestigial limbs, evidence that they evolved from a legged ancestor.


Summary

Since the dawn of history, amphibians have been a part of human culture. Western Europeans built fires for cooking and warmth, adding large logs as needed. What occasionally emerged was astounding: large black animals (which had found shelter in the logs) with four legs and a tail, jet black with striking bright yellow spots. These fire salamanders were variously thought to be the product of the fire itself, or, as Aristotle reported, capable of extinguishing fire. Pliny the Elder is said to have tested this idea by throwing a salamander into flames — the salamander died! — nevertheless the association with fire persisted. Pliny perpetuated other fantastical claims, which spread even Leonardo da Vinci contributed to the legend, and myths from different regions merged — at one point, asbestos was claimed to be salamander wool. Salamanders were attributed great powers a single salamander upstream was thought to be sufficient to kill an army. King Francis I. of France chose a salamander as his emblem — a powerful symbol, born of fire, filled with poison, immune from burning, and even able to douse flames. Before the emergence of great cities and conurbations, people grew up surrounded by nature. Salamanders and newts, toads and frogs were all part of normal human experience. Myths such as those surrounding the fire salamanders were commonplace. Shakespeare’s witches brewed with an eye of newt and tail of frog. As a child, we raised tadpoles and were taught to shudder at the appearance of a tiger salamander in a root cellar. In general, amphibians are seen as benign and harmless, even helpful as creatures that devour harmful insects and serve as an alternative food source. Thus, it came as a shock to most biologists and to the public at large in the 1980s that amphibians around the world were in decline and that they were at greater risk of extinction as a taxon than any other vertebrate group. A study of every amphibian species known in 2004 showed that on the order of 40% were at high risk of extinction, and by 2008, the decline of amphibians was seen as evidence of an impending sixth mass extinction.


About Amphibians

Mark Wilson / Getty Images

Amphibians are unique in their ability to live both on land and in water. There are about 6,200 species of amphibians on Earth today. Amphibians have certain characteristics that separate them from reptiles and other animals:

  • They are born in water and then metamorphose (change) into adults that can live on land.
  • Amphibians can breathe and absorb water through their thin skin.
  • They have many different ways of reproducing: some lay eggs, some bear live young, some carry their eggs, while still others leave their young to fend for themselves.

Results and discussion

K-mer to lowest common ancestor database

At the core of Kraken is a database that contains records consisting of a k-mer and the LCA of all organisms whose genomes contain that k-mer. This database, built using a user-specified library of genomes, allows a quick lookup of the most specific node in the taxonomic tree that is associated with a given k-mer. Sequences are classified by querying the database for each k-mer in a sequence, and then using the resulting set of LCA taxa to determine an appropriate label for the sequence (Figure 1 and Materials and methods). Sequences that have no k-mers in the database are left unclassified by Kraken. By default, Kraken builds the database with k = 31, but this value is user-modifiable.

The Kraken sequence classification algorithm. To classify a sequence, each k-mer in the sequence is mapped to the lowest common ancestor (LCA) of the genomes that contain that k-mer in a database. The taxa associated with the sequence’s k-mers, as well as the taxa’s ancestors, form a pruned subtree of the general taxonomy tree, which is used for classification. In the classification tree, each node has a weight equal to the number of k-mers in the sequence associated with the node’s taxon. Each root-to-leaf (RTL) path in the classification tree is scored by adding all weights in the path, and the maximal RTL path in the classification tree is the classification path (nodes highlighted in yellow). The leaf of this classification path (the orange, leftmost leaf in the classification tree) is the classification used for the query sequence.

Simulated metagenome data

Although genuine metagenomic reads might provide the most realistic test of performance, such data would not allow us to assess classification accuracy, because the true species in metagenomic data sets today are mostly unknown. We instead used two simulated metagenomes created by combining real sequences obtained from projects that sequenced isolated microbial genomes. When creating these simulated metagenomes, we used data sequenced by the Illumina HiSeq and MiSeq sequencing platforms, and thus we call these the HiSeq and MiSeq metagenomes, respectively (see Materials and methods). These metagenomes were constructed to measure classification speed and genus-level accuracy for data generated by current and widely used sequencing platforms.

In addition to the two simulated metagenomes constructed with sequences from isolated genomes, we created a third metagenomic sample covering a much broader range of the sequenced phylogeny. This sample, featuring simulated bacterial and archaeal reads (called simBA-5), was created with an error rate five times higher than would be expected, to evaluate Kraken’s performance on data that contain many errors or have strong differences from Kraken’s genomic library (see Materials and methods).

Classification accuracy

Classifiers generally adopt one of two strategies: for example, PhymmBL and NBC classify all sequences as accurately as possible, while Kraken and Megablast leave some sequences unclassified if insufficient evidence exists. Because PhymmBL and NBC label everything, they will tend to produce more false positives than methods like Kraken. In turn, one can expect a selective classifier to have higher precision at some cost to sensitivity. Uniquely among metagenomics classifiers, PhymmBL supplies confidence scores for its classifications, which can be used to discard low-confidence predictions and improve accuracy. Using a lower bound of 0.65 for genus-level confidence, we created a selective classifier based on PhymmBL’s predictions that we denote as PhymmBL65.

To compare Kraken’s accuracy to these of other classification methods, we classified 10,000 sequences from each of our simulated metagenomes and measured genus-level sensitivity and precision (Figure 2 and Table 1). Here, sensitivity refers to the proportion of sequences assigned to the correct genus. Precision, also known as positive predictive value, refers to the proportion of correct classifications, out of the total number of classifications attempted. Kraken’s sensitivity and precision are very close to that of Megablast. For all three metagenomes, Kraken’s sensitivity was within 2.5 percentage points of Megablast’s. The use of exact 31-base matches, however, appears to yield a higher precision for Kraken, as its precision was the highest of all classifiers for each of the three metagenomes. As may be expected, the nonselective classifiers were able to achieve slightly higher sensitivity than the selective classifiers, but at the cost of a significantly lower precision, approximately 80% versus close to 100% for Kraken.

Classification accuracy and speed comparison of classification programs for three simulated metagenomes. For each metagenome, genus precision and sensitivity are shown for five classifiers, and speed is shown for five programs (PhymmBL65 is simply a confidence-filtered version of PhymmBL’s results, and MetaPhlAn only classifies a subset of reads that map to one of its marker genes, as it is an abundance estimation program). Results shown are for: (a) the HiSeq metagenome, consisting of HiSeq reads (mean length μ = 92 bp) in equal proportion from ten bacterial sequencing projects (b) the MiSeq metagenome, consisting of MiSeq reads (μ = 156 bp) in equal proportion from ten bacterial projects and (c) the simBA-5 metagenome, consisting of simulated 100-bp reads with a high error rate from 1,967 bacterial and archaeal taxa. Note that the horizontal axes in all speed graphs have a logarithmic scale.

We also note the recent publication of a method, LMAT [12], which uses a k-mer indexing scheme similar to Kraken’s, but otherwise differs in its classification strategy. LMAT cannot easily be downloaded and run on our simulated data (see Additional file 1: Note 1) so instead we ran Kraken on a data set used for LMAT’s published results. For that data (the PhymmBL set), Kraken exceeded LMAT’s accuracy in both identifying read origin and identifying the presence of species in the sample. Both methods had essentially perfect (near 100%) precision, but Kraken correctly labelled the species of 89% of the reads while LMAT only did so for 74% of the reads. However, as we note, that data set does not provide a good basis for comparison because the reads are simulated without error from genomes included in both Kraken’s and LMAT’s databases.

Classification speed

Because of the very large size of metagenomic data sets today, classification speed is critically important, as demonstrated by the emergence of rapid abundance estimation programs such as MetaPhlAn. To evaluate classification speed, we ran each classifier, as well as MetaPhlAn, against each of the three metagenomes that we used to test accuracy (Figure 2).

Kraken classified reads much faster than any other classifier, with performance ranging from 150 to 240 times faster than the closest competitor. Kraken processed data at a rate of over 1.5 million reads per minute (rpm) for the HiSeq metagenome, over 1.3 million rpm for the simBA-5 metagenome and over 890,000 rpm for the MiSeq metagenome. The next fastest classifier, Megablast, had speeds of 7,143 rpm for the HiSeq metagenome, 4,511 rpm for the simBA-5 metagenome and 2,830 rpm for the MiSeq metagenome. For all three metagenomes, PhymmBL classified at a rate of <100 rpm and NBC at <10 rpm. Kraken is also more than three times as fast as MetaPhlAn (which only classifies a subset of reads), which had speeds of 445,000 rpm, 371,000 rpm and 276,000 rpm for the HiSeq, simBA-5 and MiSeq metagenomes, respectively. These results are shown in Figure 2. As expected, all tools processed the longer MiSeq reads (mean length μ = 156 bp) more slowly than the simBA-5 (μ = 100 bp) or HiSeq (μ = 92 bp) reads. We also performed a speed comparison against LMAT using one of the real samples discussed in LMAT’s published results on this sample Kraken was 38.82 times faster than LMAT and 7.55 times faster than a version of LMAT using a smaller database (Additional file 1: Note 1).

Other variants of Kraken

To obtain maximal speed, Kraken needs to avoid page faults (instances where data must be brought from a hard drive into physical memory), so it is important that Kraken runs on a computer with enough RAM to hold the entire database. Although Kraken’s default database requires 70 GB of RAM, we also developed a method to remove k-mers from the database, which dramatically reduces the memory requirements. We call this version of Kraken, which uses a smaller database, MiniKraken. For our results here, we used a 4 GB database. Compared to Kraken, the ability of MiniKraken to recognize species from short reads is lower, with sensitivity for our real sequence metagenomes dropping approximately 11% (Figure 3 and Table 1). On the high-error simBA-5 metagenome, MiniKraken’s sensitivity was more than 25 percentage points lower than Kraken’s, indicating that for short reads, high error rates can cause substantial loss in sensitivity. However, for all three metagenomes, MiniKraken was more precise than Kraken.

Classification accuracy and speed comparison of variants of Kraken for three simulated metagenomes. For each metagenome, genus precision and sensitivity are shown for five classifiers, and speed is shown for Kraken, along with a reduced memory version of Kraken (MiniKraken), quick execution versions of both (Kraken-Q and MiniKraken-Q), and Kraken run with a database containing draft and completed microbial genomes from GenBank (Kraken-GB). Results shown are for the same metagenomes used in Figure 2. Note that the scales of the axes differ from Figure 2, as the precision and speed of Kraken (and its variants) exceed that of the other classifiers used. (a) HiSeq metagenome. (b) MiSeq metagenome. (c) simBA-5 metagenome.

MiniKraken’s high precision demonstrates that in many cases we do not need to examine all k-mers in a sequence to get the correct classification. Taking this idea to its extreme, we developed a ‘quick operation’ mode for Kraken (and MiniKraken), where instead of querying all k-mers in a sequence against our database, we instead stop at the first k-mer that exists in the database, and use the LCA associated with that k-mer to classify the sequence. This operation mode (denoted by appending -Q to the classifier name) allows Kraken to skip tens or hundreds of k-mer queries per sequence, significantly increasing its classification speed with only a small fall in accuracy (Figure 3 and Table 1). Because a database containing fewer k-mers requires more queries from a sequence to find a hit, MiniKraken-Q is slower than Kraken-Q, even when MiniKraken is faster than Kraken.

We also created a variant Kraken database that contains GenBank’s draft and completed genomes for bacteria and archaea, which we call Kraken-GB. The regular version of Kraken only includes RefSeq complete genomes, of which there are 2,256, while Kraken-GB contains 8,517 genomes. Our hypothesis was that Kraken-GB would have a higher sensitivity than standard Kraken for our metagenomes, by virtue of its larger database. Kraken-GB has a much higher sensitivity for the HiSeq and MiSeq metagenomes compared to Kraken (Figure 3 and Table 1), primarily due to the presence of two genomes in these simulated metagenomic samples that have close relatives only in Kraken-GB’s database (Materials and methods).

Although Kraken-GB does have higher sensitivity than Kraken, it sometimes makes surprising errors, which we discovered were caused by contaminant and adapter sequences in the contigs of some draft genomes. These contaminant sequences come from other bacteria, viruses or even human genomes, and they result in incorrectly labelled k-mers in the database. We attempted to remove these from Kraken-GB (Materials and methods), but some contaminants may still slip through any filters. Thus for now, the default version of Kraken uses only complete RefSeq genomes.

Clade exclusion experiments

An important goal of metagenomics is the discovery of new organisms, and the proper classification of novel organisms is a challenge for any classifier. Although a classifier cannot possibly give a novel species the proper species label, it may be able to identify the correct genus. To simulate the presence of novel organisms, we re-analyzed the simBA-5 metagenome after first removing organisms from the Kraken database that belonged to the same clade. That is, for each read, we masked out database hits for the species of the read’s origin, and evaluated Kraken’s accuracy at the higher ranks (e.g., genus and family). We continued this masking and evaluation process for clades of origin up to the phylum rank. This procedure approximates how Kraken would classify the metagenomic reads if that clade were not present in the database.

Table 2 contains the results of this analysis. Kraken exhibited high rank-level precision in all cases where a clade was excluded, with rank-level precision remaining at or above 93% for all pairs of measured and excluded ranks. However, sensitivity was dramatically lower: at best, Kraken was able to classify approximately 33% of reads when their species has never been seen before. This is not surprising in light of Kraken's reliance on exact matches of relatively long k-mers: sequences deriving from different genera rarely share long exact matches. Nonetheless, the high precision in this experiment indicates that when Kraken is presented with novel organisms, it is likely to either classify them properly at higher levels or not classify them at all.

Human Microbiome Project data

We used Kraken to classify reads from three saliva samples collected as part of the Human Microbiome Project. Because these samples were obtained from humans, we created a Kraken database containing bacterial, viral and human genomes to classify these reads. Combining the three samples together, we report the taxonomic distribution of the classified reads (Figure 4). An analysis of the classified reads from the combined samples reveals that a majority of those reads were classified into one of three genera: Streptococcus (30%), Haemophilus (17%) and Prevotella (13%). Streptococcus mitis[13], Haemophilus parainfluenzae[14] and Prevotella melaninogenica[15], the most abundant species (by read count) of each of these three genera, are all known to be associated with human saliva. We also performed the classification on each sample separately (Additional file 1: Figures S1,S2,S3).

Taxonomic distribution of saliva microbiome reads classified by Kraken. Sequences from saliva samples collected from three individuals were classified by Kraken. The distribution of those reads that were classified by Kraken is shown.

Of note is that 68.2% of the reads were not classified by Kraken. To determine why these reads were not classified by Kraken, we aligned a randomly selected subset of 2,500 of these unclassified reads to the RefSeq bacterial genomes using BLASTN. Only 11% (275) of the subset of unclassified reads had a BLASTN alignment with E-value ≤ 10 −5 and identity ≥90%. This suggests that the vast majority of the reads not classified by Kraken were significantly different from any known species, and thus simply impossible to identify.


Evolution and biogeography of frogs and salamanders, inferred from fossils, morphology and molecules

Classified in the Lissamphibia, modern amphibians are the only non-amniote tetrapods living today. They consist of three morphologically distinct groups: the tailless frogs and toads (Anura), the limbless caecilians (Gymnophiona), and the tailed salamanders and newts (Urodela). With 205 species, the caecilians are highly specialized worm-like forms that live a fossorial lifestyle, with a relatively narrow distribution in the tropic rainforests of South America, Africa and Asia (Duellman and Trueb, 1994 Amphibiaweb, 2015). Salamanders, with 683 species, are widely distributed in the North America, Asia and Europe, with a few plethodontids extending to Central and South America (Duellman and Trueb, 1994 Amphibiaweb, 2015). Frogs are the most diverse amphibian groups, with 6644 species distributed over all continents except Antarctica (Duellman and Trueb, 1994 Amphibiaweb, 2015). Both frogs and salamanders develop a wide array of lifestyles, ranging from terrestrial, aquatic, fossorial to aboreal lifestyles (Duellman and Trueb, 1994). During ontogeny, amphibian larvae usually undergo a drastic post-embryonic shift into an adult form, a term known as metamorphosis. In salamanders, another developmental pathway – neoteny – also occurs, in which the larval morphology is retained in sexually mature adults (Duellman and Trueb, 1994 Rose, 2003). Because of the diverse lifestyles and developmental pathways, frogs and salamanders are often used as model systems in many fields of biology (e.g., evo-devo).
Over a century, but especially in the past two decades, a wealth of frog and salamander fossils has been discovered from the Mesozoic and Cenozoic of East Asia (e.g., Noble, 1924 Young, 1936 Borsuk-Bialynicka, 1978 Gao, 1986 Dong and Wang, 1998 Gao and Shubin, 2001, 2003, 2012 Gao and Wang, 2001 Gao and Chen, 2004 Wang and Rose, 2005 Wang and Evans, 2006b Zhang et al., 2009 Chen et al., 2016 this study). Some of these fossils represent the earliest members of many crown clades, including the earliest crown salamanders from the Middle Jurassic (

165 Ma, Gao and Shubin, 2003), the earliest salamandroid from the Late Jurassic, the earliest sirenid from the Late Jurassic (this study), and the earliest spadefoot toads from the late Paleocence (Chen et al., 2016). Other fossils also bear important anatomical, temporal and geographical information in understanding their evolution. Unfortunately, the importance of many of these fossils remains obscure in a phylogenetic context. For example, an early-middle Oligocene Mongolian spadefoot toad Macropelobates osborni (Noble, 1924) was discovered outside the current distribution of spadefoot toads, yet its phylogenetic position and its implication on spadefoot toad biogeography remain not well understood.
A major reason for the poor understanding of these fossils can be attributed to a trend of dichotomy between morphological and molecular phylogenies on amphibians. Whereas morphologists and paleontologists sometimes use a relatively small morphological dataset to reconstruct relationships (e.g., Gao and Shubin, 2012 Henrici, 2013), large-scale phylogenies are almost always conducted with molecular data with only living taxa (e.g., Roelants and Bossuyt, 2005 Pyron and Wiens, 2011). Very few studies on amphibian phylogeny have combined morphological and molecular data together, and even fewer also combined fossils. Because of this, the positions of many important fossils remains unclear, and the evolutionary scenarios inferred from only living species can sometimes be inconsistent with fossil evidence.
In this thesis, I adopt a total-evidence approach to understand the evolution of amphibians, especially frogs and salamanders. I will incorporate information from fossils, morphology and molecules together to reconstruct the relationships. Compared with studies with each individual datasets, this approach incorporates all available data in a single analysis, with a goal to reach robust and congruent results that allow further discussions on character evolution and biogeographic reconstruction. The inclusion of fossils directly into the combined analysis provides the time dimension that is independent from molecular data (Norell, 1992). The anatomical combination of fossils can represent intermediate forms that help to solve the “long branch” problems caused by highly specialized modern taxa. The morphological dataset, despite its much smaller size with molecular data, is the only link between fossils and modern taxa. The inclusion of key morphological characters in both reconstructing phylogenetic hypotheses and examining character evolution provide consistent results that allow discussion on the homology/homoplasy of a certain character without ambiguity. The molecular sequence data provides overwhelmingly large data on modern taxa for phylogenetic reconstructions compared with morphological data, which helps to reach a robust hypothesis. Although fossils contain no molecular data, the inclusion of molecular sequence data into the combined analysis does have an effect on the positions of fossil taxa. By altering the relationship “framework” of modern taxa, the character optimization of fossils and other taxa of a combined analysis also varies compared with results of morphology-only analysis, thus changing the positions of fossils. In the following five chapters, I will describe a number of fossil amphibian species, reconstruct three combined phylogenies, and use the results for discussions on character evolution and biogeography.
In Chapter 1 and Chapter 2, I focus on a frog clade called spadefoot toads (Anura: Pelobatoidea). In Chapter 1, I provide descriptions on three important fossil spadefoot toads from the Cenozoic of East Asia and North America: Macropelobates osborni from the early-middle Oligocene of Mongolia, Prospea holoserisca from the latest Paleocene of Mongolia, and Scaphiopus skinneri from the middle Oligocene of the United States. In Chapter 2, I conduct a combined phylogenetic analysis of archaeobatrachian frogs, and discuss the evolution of the bony spade and the historical biogeography of spadefoot toads based on the results of the phylogeny.
In Chapter 3, I describe a new fossil frog from the Early Cretaceous of Inner Mongolia, China. The unique morphology of the new fossil is distinct from previous Early Cretaceous frogs from the Jehol Biota of China. Results of the combined analysis show that the new frog represents a basal member of the Pipanura. Comparisons between the Early Cretaceous frogs from China, Spain and Brazil show a high diversity of species coupled with a high degree of endemism during the Early Cretaceous. I discuss in the phylogenetic context how early frogs gradually reach their postcranial body plan with a shortened vertebral column, loss of ribs, and specialized pelvic regions.
In Chapter 4, I provide a brief review of Mesozoic fossil salamanders from northern China, and describe a new fossil from the Late Jurassic of Liaoning Province, China. I conduct a combined phylogeny of higher-level relationships of salamanders. The new fossil, despite its general-looking appearance, represents a basal member of the highly specialized eel-like neotenic family Sirenidae on the cladogram. I discuss character evolutions in the Sirenidae, and how the neotenic developmental pathway evolved in early salamanders.
In Chapter 5, I conduct a combined phylogenetic analysis of the salamander suborder Cryptobranchoidea, consisting of the neotenic giant salamanders (Cryptobranchidae) and the metamorphic Asiatic salamanders (Hynobiidae). The new morphological matrix includes new characters that were previously less sampled in the hynobranchial region. The monophyly of the Hynobiidae are confirmed by the new analysis, and four unequivocal synapomorphies are found for the clade. An S-DIVA biogeographic reconstruction is conducted to disscuss the distributional patterns of the Hynobiidae.


Apoda: Caecilians

An estimated 185 species comprise caecilians, a group of amphibians that belong to the order Apoda. Although they are vertebrates, a complete lack of limbs leads to their resemblance to earthworms in appearance. They are adapted for a soil-burrowing or aquatic lifestyle, and they are nearly blind. These animals are found in the tropics of South America, Africa, and Southern Asia. They have vestigial limbs, evidence that they evolved from a legged ancestor.

Evolution Connection

The Paleozoic Era and the Evolution of Vertebrates The climate and geography of Earth was vastly different during the Paleozoic Era, when vertebrates arose, as compared to today. The Paleozoic spanned from approximately 542 to 251 million years ago. The landmasses on Earth were very different from those of today. Laurentia and Gondwana were continents located near the equator that subsumed much of the current day landmasses in a different configuration (Figure). At this time, sea levels were very high, probably at a level that hasn’t been reached since. As the Paleozoic progressed, glaciations created a cool global climate, but conditions warmed near the end of the first half of the Paleozoic. During the latter half of the Paleozoic, the landmasses began moving together, with the initial formation of a large northern block called Laurasia. This contained parts of what is now North America, along with Greenland, parts of Europe, and Siberia. Eventually, a single supercontinent, called Pangaea, was formed, starting in the latter third of the Paleozoic. Glaciations then began to affect Pangaea’s climate, affecting the distribution of vertebrate life.

During the Paleozoic Era, around 550 million years ago, the continent Gondwana formed. Both Gondwana and the continent Laurentia were located near the equator.

During the early Paleozoic, the amount of carbon dioxide in the atmosphere was much greater than it is today. This may have begun to change later, as land plants became more common. As the roots of land plants began to infiltrate rock and soil began to form, carbon dioxide was drawn out of the atmosphere and became trapped in the rock. This reduced the levels of carbon dioxide and increased the levels of oxygen in the atmosphere, so that by the end of the Paleozoic, atmospheric conditions were similar to those of today.

As plants became more common through the latter half of the Paleozoic, microclimates began to emerge and ecosystems began to change. As plants and ecosystems continued to grow and become more complex, vertebrates moved from the water to land. The presence of shoreline vegetation may have contributed to the movement of vertebrates onto land. One hypothesis suggests that the fins of aquatic vertebrates were used to maneuver through this vegetation, providing a precursor to the movement of fins on land and the development of limbs. The late Paleozoic was a time of diversification of vertebrates, as amniotes emerged and became two different lines that gave rise, on one hand, to mammals, and, on the other hand, to reptiles and birds. Many marine vertebrates became extinct near the end of the Devonian period, which ended about 360 million years ago, and both marine and terrestrial vertebrates were decimated by a mass extinction in the early Permian period about 250 million years ago.

Link to Learning


Background & Summary

Organisms’ life forms and ecological strategies (simply referred to as ‘traits’) reflect the outcome of continuous evolutionary pressures by biotic and abiotic factors 1,2 . Traits strongly determine the species’ ability to persist in a variety of environments, including interactions with other species 2–5 . At evolutionary time scales, the expression of new traits may create opportunities for phylogenetic lineages to explore novel niches, escape from predation or competition, and hence promote speciation by adaptive radiation 6–8 . At the ecological scale, traits are especially relevant in the study of community assembly where species coexistence is determined by different processes that influence trait composition of the community (e.g., coexisting species share more or less similar traits than expected by chance) 4,9,10 . Furthermore, species traits are linked to ecosystem functions and services necessary for human well-being (e.g., burrowing behavior alters soil properties, body size is associated with animal nutrient transport capacity, and feeding habits control food web structure) 11–14 . However, recent biodiversity loss due to anthropogenic causes raise questions about the ability of ecosystems to continue providing these benefits 15 . Therefore, understanding the mechanisms influencing patterns in trait diversity (or functional diversity), including human disturbance, is increasingly needed in face of rapid global changes 16,17 .

The last decade experienced a surge in the availability of natural history trait (i.e., morphological, ecological and reproduction traits) databases with broad taxonomic coverage 18–22 allowing unprecedented broad scale approaches in ecology and evolution 23–26 . Such data are still scarce for many amphibian species 27–29 . Amphibians are among the most diverse vertebrate groups on Earth, with more than 7,400 species and dozens of new species described every year 30 . They are abundant in many terrestrial and freshwater ecosystems, where they perform important ecosystem functions 31,32 . They are also the most threatened vertebrate group worldwide, with many species on the edge of extinction 33,34 . As such, it is urgent to improve our knowledge on amphibian traits in order to assess and predict their response to environmental changes and create conservation strategies that guarantee their survival.

In this context, we introduce AmphiBIO, an extensive database containing natural history traits for 6,775 amphibian species globally. AmphiBIO releases information on error-checked and referenced traits related to ecology, morphology and reproduction features of amphibians. Trait information was assembled from more than 1,500 literature sources, including peer-reviewed papers, existing life history databases, and other aggregated sources, in order to stimulate more comprehensive research in ecology, evolution, and conservation of amphibians. To enhance data quality, we implemented a protocol in which incorporated data were double-checked for potential errors. By making this data available to the scientific community we aim to advance the sharing of biological data and support a more integrative trait-based evolutionary and ecological science.


Author information

Affiliations

Centro de Ciencias de la Atmosfera, Universidad Nacional Autónoma de México, CDMX, Mexico

Julián A. Velasco, Francisco Estrada, Oscar Calderón-Bustamante, Carolina Ureta & Carlos Gay

Institute for Environmental Studies, VU Amsterdam, Amsterdam, the Netherlands

Programa de Investigación en Cambio Climático, Universidad Nacional Autónoma de México, CDMX, Mexico

Environnements et Paléoenvironnements Océaniques et Continentaux, CNRS, Université de Bordeaux, Pessac, France

Cátedra Consejo Nacional de Ciencia y Tecnología, CDMX, Mexico

ESPACE-DEV, Univ Montpellier, IRD, Univ Guyane, Univ Reunion, Univ Antilles, Univ Avignon, Maison de la Télédétection, Montpellier, Cedex, France

The Climate Data Factory, Paris, France

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Contributions

J.A.V. and F.E. contributed equally to the conceptual design J.A.V., F.E., O.C.B., D.S., D.D., and C.U. analyzed data. J.A.V. and F.E. wrote the paper and D.S., O.C.B., C.G., and C.U. contributed to it. All authors discussed the results and commented on the manuscript.

Corresponding author


152 Amphibians

By the end of this section, you will be able to do the following:

  • Describe the important difference between the life cycle of amphibians and the life cycles of other vertebrates
  • Distinguish between the characteristics of Urodela, Anura, and Apoda
  • Describe the evolutionary history of amphibians

Amphibians are vertebrate tetrapods (“four limbs”), and include frogs, salamanders, and caecilians. The term “amphibian” loosely translates from the Greek as “dual life,” which is a reference to the metamorphosis that many frogs and salamanders undergo and the unique mix of aquatic and terrestrial phases that are required in their life cycle. In fact, they cannot stray far from water because their reproduction is intimately tied to aqueous environments. Amphibians evolved during the Devonian period and were the earliest terrestrial tetrapods. They represent an evolutionary transition from water to land that occurred over many millions of years. Thus, the Amphibia are the only living true vertebrates that have made a transition from water to land in both their ontogeny (life development) and phylogeny (evolution). They have not changed much in morphology over the past 350 million years!

Watch this series of five Animal Planet videos on tetrapod evolution:

    1: The evolution from fish to earliest tetrapod

Characteristics of Amphibians

As tetrapods, most amphibians are characterized by four well-developed limbs. In some species of salamanders, hindlimbs are reduced or absent, but all caecilians are (secondarily) limbless. An important characteristic of extant amphibians is a moist, permeable skin that is achieved via mucus glands. Most water is taken in across the skin rather than by drinking. The skin is also one of three respiratory surfaces used by amphibians. The other two are the lungs and the buccal (mouth) cavity. Air is taken first into the mouth through the nostrils, and then pushed by positive pressure into the lungs by elevating the throat and closing the nostrils.

All extant adult amphibians are carnivorous, and some terrestrial amphibians have a sticky tongue used to capture prey. Amphibians also have multiple small teeth at the edge of the jaws. In salamanders and caecilians, teeth are present in both jaws, sometimes in multiple rows. In frogs and toads, teeth are seen only in the upper jaw. Additional teeth, called vomerine teeth , may be found in the roof of the mouth. Amphibian teeth are pedicellate, which means that the root and crown are calcified, separated by a zone of noncalcified tissue.

Amphibians have image-forming eyes and color vision. Ears are best developed in frogs and toads, which vocalize to communicate. Frogs use separate regions of the inner ear for detecting higher and lower sounds: the papilla amphibiorum, which is sensitive to frequencies below 10,000 hertz and unique to amphibians, and the papilla basilaris, which is sensitive to higher frequencies, including mating calls, transmitted from the eardrum through the stapes bone. Amphibians also have an extra bone in the ear, the operculum, which transmits low-frequency vibrations from the forelimbs and shoulders to the inner ear, and may be used for the detection of seismic signals.

Evolution of Amphibians

The fossil record provides evidence of the first tetrapods: now-extinct amphibian species dating to nearly 400 million years ago. Evolution of tetrapods from lobe-finned freshwater fishes (similar to coelacanths and lungfish) represented a significant change in body plan from one suited to organisms that respired and swam in water, to organisms that breathed air and moved onto land these changes occurred over a span of 50 million years during the Devonian period.

Aquatic tetrapods of the Devonian period include Ichthyostega and Acanthostega. Both were aquatic, and may have had both gills and lungs. They also had four limbs, with the skeletal structure of limbs found in present-day tetrapods, including amphibians. However, the limbs could not be pulled in under the body and would not have supported their bodies well out of water. They probably lived in shallow freshwater environments, and may have taken brief terrestrial excursions, much like “walking” catfish do today in Florida. In Ichthyostega, the forelimbs were more developed than the hind limbs, so it might have dragged itself along when it ventured onto land. What preceded Acanthostega and Ichthyostega?

In 2006, researchers published news of their discovery of a fossil of a “tetrapod-like fish,” Tiktaalik roseae, which seems to be a morphologically “intermediate form” between sarcopterygian fishes having feet-like fins and early tetrapods having true limbs ((Figure)). Tiktaalik likely lived in a shallow water environment about 375 million years ago. 1 Tiktaalik also had gills and lungs, but the loss of some gill elements gave it a neck, which would have allowed its head to move sideways for feeding. The eyes were on top of the head. It had fins, but the attachment of the fin bones to the shoulder suggested they might be weight-bearing. Tiktaalik preceded Acanthostega and Ichthyostega, with their four limbs, by about 10 million years and is considered to be a true intermediate clade between fish and amphibians.


The early tetrapods that moved onto land had access to new nutrient sources and relatively few predators. This led to the widespread distribution of tetrapods during the early Carboniferous period, a period sometimes called the “age of the amphibians.”

Modern Amphibians

Amphibia comprises an estimated 6,770 extant species that inhabit tropical and temperate regions around the world. All living species are classified in the subclass Lissamphibia (“smooth-amphibian”), which is divided into three clades: Urodela (“tailed”), the salamanders Anura (“tail-less”), the frogs and Apoda (“legless ones”), the caecilians.

Urodela: Salamanders

Salamanders are amphibians that belong to the order Urodela (or Caudata). These animals are probably the most similar to ancestral amphibians. Living salamanders ((Figure)) include approximately 620 species, some of which are aquatic, others terrestrial, and some that live on land only as adults. Most adult salamanders have a generalized tetrapod body plan with four limbs and a tail. The placement of their legs makes it difficult to lift their bodies off the ground and they move by bending their bodies from side to side, called lateral undulation, in a fish-like manner while “walking” their arms and legs fore-and-aft. It is thought that their gait is similar to that used by early tetrapods. The majority of salamanders are lungless, and respiration occurs through the skin or through external gills in aquatic species. Some terrestrial salamanders have primitive lungs a few species have both gills and lungs. The giant Japanese salamander, the largest living amphibian, has additional folds in its skin that enlarge its respiratory surface.

Most salamanders reproduce using an unusual process of internal fertilization of the eggs. Mating between salamanders typically involves an elaborate and often prolonged courtship. Such a courtship ends in the deposition of sperm by the males in a packet called a spermatophore , which is subsequently picked up by the female, thus ultimately fertilization is internal. All salamanders except one, the fire salamander, are oviparous. Aquatic salamanders lay their eggs in water, where they develop into legless larvae called efts. Terrestrial salamanders lay their eggs in damp nests, where the eggs are guarded by their mothers. These embryos go through the larval stage and complete metamorphosis before hatching into tiny adult forms. One aquatic salamander, the Mexican axolotl, never leaves the larval stage, becoming sexually mature without metamorphosis.


View River Monsters: Fish With Arms and Hands? to see a video about an unusually large salamander species.

Anura: Frogs

Frogs ((Figure)) are amphibians that belong to the order Anura or Salientia (“jumpers”). Anurans are among the most diverse groups of vertebrates, with approximately 5,965 species that occur on all of the continents except Antarctica. Anurans, ranging from the minute New Guinea frog at 7 mm to the huge goliath frog at 32 cm from tropical Africa, have a body plan that is more specialized for movement. Adult frogs use their hind limbs and their arrow-like endoskeleton to jump accurately to capture prey on land. Tree frogs have hands adapted for grasping branches as they climb. In tropical areas, “flying frogs” can glide from perch to perch on the extended webs of their feet. Frogs have a number of modifications that allow them to avoid predators, including skin that acts as camouflage. Many species of frogs and salamanders also release defensive chemicals that are poisonous to predators from glands in the skin. Frogs with more toxic skins have bright warning (aposematic) coloration.


Frog eggs are fertilized externally, and like other amphibians, frogs generally lay their eggs in moist environments. Although amphibian eggs are protected by a thick jelly layer, they would still dehydrate quickly in a dry environment. Frogs demonstrate a great diversity of parental behaviors, with some species laying many eggs and exhibiting little parental care, to species that carry eggs and tadpoles on their hind legs or embedded in their backs. The males of Darwin’s frog carry tadpoles in their vocal sac. Many tree frogs lay their eggs off the ground in a folded leaf located over water so that the tadpoles can drop into the water as they hatch.

The life cycle of most frogs, as other amphibians, consists of two distinct stages: the larval stage followed by metamorphosis to an adult stage. However, the eggs of frogs in the genus Eleutherodactylus develop directly into little froglets, guarded by a parent. The larval stage of a frog, the tadpole, is often a filter-feeding herbivore. Tadpoles usually have gills, a lateral line system, longfinned tails, and lack limbs. At the end of the tadpole stage, frogs undergo metamorphosis into the adult form ((Figure)). During this stage, the gills, tail, and lateral line system disappear, and four limbs develop. The jaws become larger and are suited for carnivorous feeding, and the digestive system transforms into the typical short gut of a predator. An eardrum and air-breathing lungs also develop. These changes during metamorphosis allow the larvae to move onto land in the adult stage.


Apoda: Caecilians

An estimated 185 species comprise the caecilians , a group of amphibians that belong to the order Apoda. They have no limbs, although they evolved from a legged vertebrate ancestor. The complete lack of limbs makes them resemble earthworms. This resemblance is enhanced by folds of skin that look like the segments of an earthworm. However, unlike earthworms, they have teeth in both jaws, and feed on a variety of small organisms found in soil, including earthworms! Caecilians are adapted for a burrowing or aquatic lifestyle, and they are nearly blind, with their tiny eyes sometimes covered by skin. Although they have a single lung, they also depend on cutaneous respiration. These animals are found in the tropics of South America, Africa, and Southern Asia. In the caecelians, the only amphibians in which the males have copulatory structures, fertilization is internal. Some caecilians are oviparous, but most bear live young. In these cases, the females help nourish their young with tissue from their oviduct before birth and from their skin after birth.

The Paleozoic Era and the Evolution of Vertebrates When the vertebrates arose during the Paleozoic Era (542 to 251 MYA), the climate and geography of Earth was vastly different. The distribution of landmasses on Earth were also very different from that of today. Near the equator were two large supercontinents, Laurentia and Gondwana , which included most of today’s continents, but in a radically different configuration ((Figure)). At this time, sea levels were very high, probably at a level that hasn’t been reached since. As the Paleozoic progressed, glaciations created a cool global climate, but conditions warmed near the end of the first half of the Paleozoic. During the latter half of the Paleozoic, the landmasses began moving together, with the initial formation of a large northern block called Laurasia , which contained parts of what is now North America, along with Greenland, parts of Europe, and Siberia. Eventually, a single supercontinent, called Pangaea , was formed, starting in the latter third of the Paleozoic. Glaciations then began to affect Pangaea’s climate and the distribution of vertebrate life.


During the early Paleozoic, the amount of carbon dioxide in the atmosphere was much greater than it is today. This may have begun to change later, as land plants became more common. As the roots of land plants began to infiltrate rock and soil began to form, carbon dioxide was drawn out of the atmosphere and became trapped in the rock. This reduced the levels of carbon dioxide and increased the levels of oxygen in the atmosphere, so that by the end of the Paleozoic, atmospheric conditions were similar to those of today.

As plants became more common through the latter half of the Paleozoic, microclimates began to emerge and ecosystems began to change. As plants and ecosystems continued to grow and become more complex, vertebrates moved from the water to land. The presence of shoreline vegetation may have contributed to the movement of vertebrates onto land. One hypothesis suggests that the fins of aquatic vertebrates were used to maneuver through this vegetation, providing a precursor to the movement of fins on land and the further development of limbs. The late Paleozoic was a time of diversification of vertebrates, as amniotes emerged and became two different lines that gave rise, on one hand, to synapsids and mammals, and, on the other hand, to the codonts, reptiles, dinosaurs, and birds. Many marine vertebrates became extinct near the end of the Devonian period, which ended about 360 million years ago, and both marine and terrestrial vertebrates were decimated by a mass extinction in the early Permian period about 250 million years ago.

Section Summary

As tetrapods, most amphibians are characterized by four well-developed limbs, although some species of salamanders and all caecilians are limbless. The most important characteristic of extant amphibians is a moist, permeable skin used for cutaneous respiration, although lungs are found in the adults of many species.

All amphibians are carnivores and possess many small teeth. The fossil record provides evidence of amphibian species, now extinct, that arose over 400 million years ago as the first tetrapods. Living Amphibia can be divided into three classes: salamanders (Urodela), frogs (Anura), and caecilians (Apoda). In the majority of amphibians, development occurs in two distinct stages: a gilled aquatic larval stage that metamorphoses into an adult stage, acquiring lungs and legs, and losing the tail in Anurans. A few species in all three clades bypass a free-living larval stage. Various levels of parental care are seen in the amphibians.


'Dead clades walking': Fossil record provides new insights into mass extinctions

Mass extinctions are known as times of global upheaval, causing rapid losses in biodiversity that wipe out entire animal groups. Some of the doomed groups linger on before going extinct, and a team of scientists found these "dead clades walking" (DCW) are more common and long-lasting than expected.

"Dead clades walking are a pattern in the fossil record where some animal groups make it past the extinction event, but they also can't succeed in the aftermath," said Benjamin Barnes, a doctoral student in geosciences at Penn State. "It paints the pictures of a group consigned to an eventual extinction."

The scientists found 70 of the 134 orders of ancient sea-dwelling invertebrates they examined could be identified as DCW in a new statistical analysis of the fossil record.

"What really fascinated us was that over half of all the orders we looked at have this phenomenon and that it can look like many different things," said Barnes, who led a group of graduate students and a postdoctoral researcher on the study. "In some cases, you have a group that has a sudden drop in diversity and lasts for a few more million years before disappearing from the record. But we also found many orders straggled along sometimes for tens or hundreds of millions of years."

The findings, published in the journal Proceedings of the National Academy of Sciences, challenge the view of extinction as a sudden disappearance and suggest that the full impact of mass extinctions lag behind the events themselves longer than previously expected, the scientists said.

"I think it raises questions about how the so-called kill mechanism operates," Barnes said. "We think of mass extinctions as being these selective forces that cause large groups of animals to go extinct, but our results really show there are a lot of instances where it's not so sudden. It raises questions about why that's such a long delay."

Paleontologist David Jablonski first coined the term DCW more than 20 years ago, and since then it has been associated almost exclusively with mass extinctions. Using a wealth of new fossil record data made available over the last two decades, the study found DCW are also common around smaller, more localized background extinction stages, the scientists said.

"Our results suggest that rather than representing a rare, brief fossil pattern in the wake of mass extinction events, DCWs are actually a really diverse phenomenon and that there might be a lot of drivers that produce this pattern in the fossil record," Barnes said. "These DCWs may represent a major macroevolutionary pattern."

The scientists used a statistical technique called a Bayesian change point algorithm to analyze fossil records from the Paleobiology Database, a public record of paleontological data maintained by international scientists.

The method allowed the researchers to search time series data for significant points where the data deviated from the pattern. They were able to identify negative jagged shifts in diversity and rule out that the organism went extinct immediately but instead persisted.

"So you might be looking in the fossil record and you'll find tons of a type of brachiopod," Barnes said. "Each order has a handful of families and dozens of genera within those families. Then you might see a drop in diversity, and the majority of those genera disappear and perhaps there's only one family that continues to survive."

Those survivors can continue in their niche for millions of years, even into the present. But their lack of diversity makes them more susceptible to future environmental challenges or extinction events, the scientists said.

"I think these findings cause you to reexamine how you measure success," Barnes said. "It's quite possible for an animal group not to produce new families and new genera at a rate like it did before, but if it continues to survive for many millions of years, that's still some form of success. I think it raises a lot of questions about what it means to be successful as a fossil organism and what ultimately are the controls of origination."


Watch the video: Amphibians. locomotion in Amphibians. Biology Plus. Lecture #24 (December 2022).