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Write Essays On Origin Of Tetrapods During Devonian

Originally published in Journal of Creation 17, no 2 (August 2003): 111-117.

According to evolutionary theory, the origin of tetrapods from a fish-like ancestor during the Devonian Period was one of the major events in the history of life on earth.

Summary

According to evolutionary theory, the origin of tetrapods from a fish-like ancestor during the Devonian Period was one of the major events in the history of life on earth. The ‘drying pond’ hypothesis was proposed to explain the selection pressures behind the transition. According to this hypothesis, the tetrapods evolved as fishes became progressively better adapted to terrestrial conditions during prolonged episodes of drought. Recently, however, the assumption that feet and legs evolved to facilitate life on the land has been called into question. The ‘earliest’ known tetrapods with feet and legs are now thought to have been aquatic animals; evolutionists therefore argue that feet and legs evolved in a shallow water environment and were only later co-opted for use on the land. This paper reviews the radical changes in thinking about the fish-tetrapod transition that have taken place in the evolutionary community. It also considers the chimeromorphic nature of Devonian tetrapods and fishes, and offers some critical comments on the evolutionary interpretation of their fossil record.

Evolutionists believe that tetrapods—i.e. vertebrates with four limbs—were the first animals to move on to the land, having evolved from a fish ancestor during the Devonian period (conventionally 408 to 360 million years ago). The fossil record of Devonian tetrapods is often presented as compelling evidence of this major evolutionary transition.1 Science writer Carl Zimmer has written a popular book, At the Water’s Edge,2 which purports to show how life came ashore (i.e. how fish evolved into tetrapods) and then went back to the sea (i.e. how land mammals gave rise to the whales). A more technical presentation was written recently by Jenny Clack, Reader in Vertebrate Palaeontology and Senior Assistant Curator of the University Museum of Zoology, Cambridge. Entitled Gaining Ground: The Origin and Evolution of Tetrapods,3 it begins with these words:

‘About 370 million years ago, something strange and significant happened on Earth. That time, part of an interval of Earth’s history called the Devonian Period by scientists such as geologists and paleontologists, is known popularly as the Age of Fishes. After about 200 million years of earlier evolution, the vertebrates—animals with backbones—had produced an explosion of fishlike animals that lived in the lakes, rivers, lagoons, and estuaries of the time. The strange thing that happened during the later parts of the Devonian period is that some of these fishlike animals evolved limbs with digits—fingers and toes. Over the ensuing 350 million years or so, these so-called tetrapods gradually evolved from their aquatic ancestry into walking terrestrial vertebrates, and these have dominated the land since their own explosive radiation allowed them to colonize and exploit the land and its opportunities. The tetrapods, with their limbs, fingers, and toes, include humans, so this distant Devonian event is profoundly significant for humans as well as for the planet.’4

Indeed, according to the cladistic framework that now dominates evolutionary systematics, humans are not simply descended from fish—they are fish! Clack states:

‘Although humans do not usually think of themselves as fishes, they nonetheless share several fundamental characters that unite them inextricably with their relatives among the fishes … Tetrapods did not evolve from sarcopterygians [lobe-finned fishes]; they are sarcopterygians, just as one would not say that humans evolved from mammals; they are mammals.’5

In this paper I will critically examine the fossil record of ‘early’ tetrapods and discuss the way in which older evolutionary views of their origin have been overturned in the last two decades. I will also consider the mosaic distribution of characters that we observe in Devonian tetrapods and fishes, the problems that it poses for evolutionary theory, and how it might be understood in a creationist framework.

The ‘drying pond’ hypothesis

Many evolutionary scenarios have been proposed to explain the origin of tetrapods. Most of them were developed to answer the question, ‘Why did fish leave the water and come onto the land?’ The early theories usually focused on the environmental setting and selection pressures behind the transition. Tetrapods were thought to have evolved during the Devonian, a period associated in many parts of the world with sediments stained red by iron oxide. Classic red beds, such as the Siluro-Devonian rocks of Europe (the Old Red Sandstone) and their North American equivalents (the Catskill and Escuminac formations), have often been interpreted as the product of hot, semi-desert environments with seasonal wetness. This led many to speculate that an increasingly arid climate was a major influence on the evolution of air-breathing vertebrates. A classic paper by Barrell6 set the scene for much future discussion. He argued that the first tetrapods arose ‘under the compulsion of seasonal dryness’.7 Under such conditions, it was suggested, the air-bladder of certain fishes became progressively better adapted as an organ of respiration and the gills atrophied. The development of a new system of breathing allowed fishes to survive the drought conditions by moving between bodies of water. Those fishes with more limb-like appendages were better able to make the journey and this ultimately led to the evolution of limbs with digits. This became known as ‘the drying pond hypothesis’ and was popularized by the great vertebrate palaeontologist Alfred Sherwood Romer.8

‘Early’ tetrapods from East Greenland

When Romer was popularizing the ‘drying pond’ idea, the earliest known tetrapods were Ichthyostega and Acanthostega from the Upper Devonian of East Greenland. Ichthyostega was first described by Säve-Söderbergh9 and then by Jarvik in a series of papers and a monograph.10–12 Although the anatomy of Ichthyostega is known in considerable detail, its body proportions are uncertain because the fossil material comes from more than one individual. Ichthyostega is about one metre long with a broad, flat head, short, barrel-shaped body, stocky legs, large pelvic and pectoral girdles, and a rib cage with broad, overlapping ribs (Figure 1). It is very evidently a tetrapod, with limbs rather than fins. Nevertheless, Ichthyostega has some fish-like characteristics, including a lateral line system and a tail with bony fin rays. Early reconstructions portrayed Ichthyostega as a semi-aquatic creature but most later ones depicted it as a predominantly terrestrial animal (e.g. Jarvik13). As recently as 1988, a major vertebrate palaeontology text described Ichthyostega as a fairly typical land animal with the usual complement of five digits on the hind limb.14 The second Devonian tetrapod from East Greenland was Acanthostega.9,10 For many years this animal was known only from two partial skull roofs, but these were enough to mark it out as different from Ichthyostega.

The search for evolutionary ancestors

Evolutionists sought the ancestry of the tetrapods among the lobe-finned fishes. Although the lobe-fins are dominant in the fossil fish faunas of the Palaeozoic (conventionally 590 to 248 million years ago), they are represented today by only four surviving genera (the coelacanth Latimeria and three genera of lungfish). In 1892, Cope and others argued that tetrapods had evolved from the crossopterygians, the group of lobe-fins that includes the coelacanths.16 Various crossopterygians were proposed as the ‘model ancestor’, including Sauripteris17,18 and Osteolepis.19 However, most attention settled upon Eusthenopteron, from Escuminac Bay in Quebec, Canada. This is the fish that was commonly illustrated, in popular books on fossils, as hauling itself up onto Devonian riverbanks (e.g. Owen20).

Nevertheless, there was evidently a substantial discontinuity in the fossil record between terrestrial vertebrates like Ichthyostega and their presumed ancestors. This was reflected in creationist treatments of the problem21 and acknowledged by evolutionists, such as Carroll22 who wrote:

‘We have not found any fossils that are intermediate between such clearly terrestrial animals and the strictly aquatic rhipidistians described in the previous chapter.’

TaxonStratigraphic unitAgeLocationMaterial Reference(s)
PederpesBallagan FmTournaisianScotlandSkull, almost complete articulated skeleton23
SinostegaZhongning FmFamennianNingxia Hui, ChinaIncomplete left mandible24
TulerpetonKhovanshchina BedsFamennianTula Region, RussiaFore and hind limbs, partial pectoral and pelvic girdles, skull fragments25–28
VentastegaKetleri FmFamennianLatviaSkull fragments, girdle fragments29
AcanthostegaBritta Dal FmFamennianEast GreenlandSkulls, articulated skeletons9,10,30–36,44,50
IchthyostegaAina Dal Fm Britta Dal FmFamennianEast GreenlandSkulls, skeletal elements, some articulated9–12,44
HynerpetonCatskill FmFamennianPennsylvania, USAPectoral girdle, skull fragments37,38
DensignathusCatskill FmFamennianPennsylvania, USALower jaw38
MetaxygnathusCloghnan ShaleFamennianNew South Wales, AustraliaLower jaw39
ElginerpetonScat Craig BedsFrasnianScotlandIlia, limb bones, skull and pectoral girdle fragments40–42
ObruchevichthysOgre BedsFrasnianLatviaLower jaw fragments40
LivonianaGauja FmGivetianLatviaLower jaw fragments 43

Aquatic tetrapods challenge the ‘drying pond’ hypothesis

Since 1990 our knowledge of ‘early’ tetrapods has been greatly expanded, with many new taxa being described. Fossil material is now known from Scotland, Greenland, Latvia, the USA, Australia, Russia, and China (Table 1).23–43 Furthermore, our understanding of the Greenland tetrapods has been revolutionized by the discovery of new material. As a consequence, a major re-evaluation of tetrapod origins has taken place, and almost every aspect of the ‘drying pond’ hypothesis has had to be discarded.

The fatal blow to the ‘drying pond’ hypothesis has been the realization that the Devonian tetrapods were predominantly aquatic in habit. New ichthyostegid material, including a well-preserved and articulated hind limb, collected by an expedition to East Greenland in 1987, revealed that Ichthyostega was polydactylous, with seven digits on the hind limb (Figure 1).44 This was a very surprising discovery because pentadactyly had been assumed to be the normal condition in ‘early’ tetrapods. Furthermore, the flattened bones and inflexible ankle of the hind limb suggests that it was more like the paddle of an elephant seal than the leg of a terrestrial animal.45 It appears that the earliest reconstruction of Ichthyostega as a creature at home in the water was more accurate than later ones portraying it on land.

Acanthostega is also much more completely known as a result of material collected by the 1987 expedition, including the first postcranial remains.47,48 It was a smaller animal than Ichthyostega and its teeth suggest that it had a different diet. Several articulated specimens were found in a single lens of rock, interpreted as a possible flash flood deposit.49 The remarkable preservation meant that some delicate structures, not often preserved in fossil tetrapods, are known in Acanthostega. The gill skeleton was fish-like50 and it has been suggested that Acanthostega had internal gills somewhat similar to those of the Australian lungfish (Neoceratodus). Acanthostega had a tail with fin rays, even larger than that of Ichthyostega (Figure 2). The fin rays also extended further beneath the tail, in similar fashion to those of a lungfish, suggesting that Acanthostega was a thoroughly aquatic creature. This conclusion is supported by the morphology of the fore and hind limbs which are difficult to interpret as load-bearing structures; rather, they appear to be designed for swimming. As with Ichthyostega, perhaps the most extraordinary feature was the number of digits. An articulated fore limb revealed eight digits in a paddle-like arrangement (Figure 3). Clack51 speculates that they may have been enclosed in some kind of webbing.

Most evolutionists had assumed that the origin of limbs with digits was synonymous with the vertebrate invasion of the land. This led to the popular ‘conquest of the land’ idea, typified by artistic reconstructions and museum displays of fish crawling out of Devonian pools. However, the latest thinking about the aquatic or semi-aquatic nature of the Devonian tetrapods has led modern-day evolutionists to reject this assumption. They now argue that the key tetrapod characters evolved for a shallow-water existence and were only later co-opted for terrestrial use. The new generation of Darwinists dismisses the ‘drying pond’ hypothesis as untestable story-telling, and increasingly relies on cladistics as an alternative framework for understanding the transition. The cladistic approach to the fish-tetrapod transition focuses on determining the sequence of acquisition of key tetrapod characteristics, from which inferences are drawn about the nature of the transition.53 We should recognize, however, that the cladistic methodology is inherently Darwinian and assumes from the outset the continuity of life. By its very nature, cladistics is insensitive to the discontinuities which creationists believe characterize living things.54

Other problems with the ‘drying pond’ hypothesis

The drying pond hypothesis has other problems.55 For instance, it is recognized that red beds are not necessarily indicators of arid climates:

‘The red bed problem has been extremely controversial, with marked differences of opinion, possibly due to the fact that the term “red bed” is a catchall for many sedimentary types produced under different conditions, the only common feature of them being the red color.’56

Modern red beds develop in the oxidizing conditions of the low latitude tropics (e.g. the Amazon Basin). Such environments are characterized by monsoonal rainfall, not arid conditions. Another problem is that, even if the red beds were laid down under conditions of semi-aridity, evolutionists cannot assume that the tetrapods arose in such environments, for the simple reason that many Devonian sediments are not red beds. Some are interpreted as river, lake, or near-shore sediments rich in organic matter, suggesting nearby forests.57

Furthermore, a survey of modern fishes that leave the water to spend time on land58 affords no support for the ‘drying pond’ hypothesis. There is no association between those that leave the water and those that possess digit-like fins. For example, eels undertake long journeys overland but they have nothing that could be described as digit-like appendages. Indeed, most of the fishes that possess digit-like structures are deep water species or habitual bottom dwellers, such as the Sargassum frogfish.

New views on tetrapod ancestry

There have also been changes of opinion about which group of fishes is closest to the ancestry of tetrapods. Eusthenopteron is no longer regarded as the model ancestor. Depictions showing this fish emerging onto dry land owed more to evolutionary presuppositions than evidence. Eusthenopteron was a rather undistinguished fish with no obvious adaptations to terrestrial life; tetrapod-like behaviour was attributed to it simply because there was no better candidate to fill the role of tetrapod ancestor. The true lifestyle of Eusthenopteron seems to have been that of a lurking aquatic predator, somewhat similar to the modern pike (Esox).

Attention is now focused on the formerly more obscure lobe-finned fishes, Panderichthys and Elpistostege. Until recently, these two genera were united in a family called the panderichthyids, but evolutionists now believe that they are not uniquely related to each other.59 Fossil material from Latvia and Canada shows that these fish were more tetrapod-like than other lobe-fins. Indeed, based on a partial skull roof, Elpistostege was originally described as a tetrapod.60 Although there has been dissent,61,62 these genera are increasingly regarded by evolutionists as the closest known relatives of tetrapods.63–65 The latest work by Ahlberg et al.43 indicates that Elpistostege is even more tetrapod-like than Panderichthys. These fish have crocodile-like skulls with dorsally placed eyes, straight tails, and slightly flattened bodies without dorsal or anal fins (see Figure 4). Like tetrapods, but unlike all other fishes, they also have frontal bones in the skull roof. Like Eusthenopteron, they seem designed for life as shallow-water predators.

Chimeromorphs pose problems for evolutionary theory

Creationists and evolutionists have observed that many organisms, both fossil and living, exhibit a mosaic distribution of character traits. Parker66 put it this way:

‘Each created kind is a unique combination of traits that are individually shared with members of other groups.’

Stephen Jay Gould called such organisms ‘mosaic forms’ or ‘chimeras’67 while Kurt Wise68,69 calls them chimeromorphs. The duck-billed platypus (Ornithorhynchus anatinus), for instance, has features of both mammals (hair, milk production) and reptiles (egg-laying). Perhaps the best-known fossil example is Archaeopteryx, which combines feathers with teeth and wing claws. In fact, a mosaic pattern of character distribution is seen in many other fossil organisms. For instance, Woodmorappe70 recently drew attention to the chimeric nature of the pakicetids, a group of terrestrial artiodactyls with a whale-like inner ear.

This observation seems to apply to the Devonian tetrapods and fishes considered in this article. For example, Daeschler et al. noted that:

‘Devonian tetrapods show a mosaic of terrestrial and aquatic adaptations.’71

Some of the fishes possess tetrapod-like characters while the tetrapods have fish-like features. Evolutionists interpret mosaic organisms like these as evolutionary intermediates linking major groups. However, Wise72 makes an important point against this interpretation:

‘Although the entire organism is intermediate in structure, it’s the combination of structures that is intermediate, not the nature of the structures themselves. Each of these organisms appears to be a fully functional organism full of fully functional structures.’

Evolutionary theory might lead us to expect examples of intermediate structures, but there is nothing intermediate about, for example, the internal gills of Acanthostega, its lateral line system, or its limbs. They are fully developed and highly complex. What is unusual is their combination in a single organism. Intelligent design offers an alternative understanding of this widespread pattern. The Devonian tetrapods are thought to have lived a predatory lifestyle in weed-infested shallow water. They were therefore equipped with characteristics appropriate to that habitat (e.g. crocodile-like morphology with dorsally placed eyes, limbs and tails made for swimming, internal gills, lateral line systems). Some of these features are also found in fishes that shared their environment.

The mosaic pattern makes it difficult to identify organisms or groups of organisms that possess the ‘right’ combination of characters to be considered part of an evolutionary lineage. Consider the tetrapod-like lobe-fins Panderichthys and Elpistostege. Despite their appearance, these fish have some unique characters (such as the design of the vertebrae) that rule them out as tetrapod ancestors. At best, evolutionists can only claim that they are a model of the kind of fish that must have served as that ancestor. The same problem is encountered with the Devonian tetrapods. For example, Ichthyostega is described as ‘a very strange animal, and parts of it are like no other known tetrapod or fish’.73 Similarly, the shoulder girdles of the Devonian tetrapods ‘are not obviously halfway in structure between those of fishes and those of later tetrapods but have some unique and some unexpected features’.74 Another example is Livoniana, a so-called ‘near tetrapod’ known from two lower jaw fragments. It possesses a curious mixture of fish-like and tetrapod-like characteristics, but it also has up to five rows of teeth, a feature not seen either in the fishes from which it is thought to be descended nor the tetrapods into which it is said to be evolving.75 That the mosaic distribution of characters can cause great confusion is exemplified by the recent discovery of Psarolepis, a fish from the Upper Silurian/Lower Devonian of China, which combines characters found in placoderms, chondrichthyans, ray finned fishes, and lobe-fins.76

Additional problems with ‘early’ tetrapod evolution

Another problem is that the fossil record imposes tight constraints on the timing of the supposed transition. The earliest tetrapod fossils are found in late Frasnian sediments, but their presumed ancestors are hardly much older. To exacerbate the situation, the Frasnian ‘near tetrapods’ (Obruchevichthys, Elginerpeton, Livoniana) are already morphologically diverse at their first appearance.77 Thus Darwinists are compelled to postulate a rapid burst of evolution in which radical changes must have taken place:

Panderichthys and Elpistostege flourished in the early Frasnian and are some of the nearest relatives of tetrapods. But tetrapods appear only about 5 to 10 million years later in the late Frasnian, by which time they were widely distributed and had evolved into several groups, including the lineage leading to the tetrapods of the Famennian. This suggests that the transition from fish to tetrapod occurred rapidly within this restricted time span.’78

Second, key morphological transitions, such as the purported change from paired fins to limbs with digits, remain undocumented by fossils. Where appendages are known they are clearly either fish-like fins or digit-bearing limbs, not at some transitional stage from one to the other. At one time it was claimed that the pectoral fins of rhizodonts, a group of lobe-finned fish, were remarkably similar to tetrapod limbs, but following the description of Gooloogongia from the Famennian of New South Wales, Johanson and Ahlberg79 have urged that they not be used as a model for the origin of tetrapod limbs. Furthermore, the pectoral fins of lobe-finned fish tend to be larger than the pelvic fins, whereas the Devonian tetrapods were ‘rear-wheel drive’ animals with larger hind limbs than fore limbs.80 None of the recent fossil discoveries shed any light on this supposed reconfiguration.

Third, there are functional challenges to Darwinian interpretations. For instance, in fish the head, shoulder girdle, and circulatory systems constitute a single mechanical unit. The shoulder girdle is firmly connected to the vertebral column and is an anchor for the muscles involved in lateral undulation of the body, mouth opening, heart contractions, and timing of the blood circulation through the gills.81 However, in amphibians the head is not connected to the shoulder girdle, in order to allow effective terrestrial feeding and locomotion. Evolutionists must suppose that the head became incrementally detached from the shoulder girdle, in a step-wise fashion, with functional intermediates at every stage. However, a satisfactory account of how this might have happened has never been given.

Conclusion

Recent discoveries have undoubtedly advanced our knowledge of Devonian tetrapods and future creationist discussions of tetrapod origins must take this into account. It is no longer sufficient for creationists to contrast Eusthenopteron with Ichthyostega and point to the large morphological gap between them. We need to have more to say. Nevertheless, the presumed transition from fish to tetrapods remains contentious. The data and their interpretation are a source of lively debate and ongoing controversy:

‘In the not-too-distant past, there was almost no fossil material, and ideas were based largely on informed guesswork. Speculation was intense, and as is often the case, in inverse proportion to the amount of data. To be truthful, there is still not much real data, so that speculation is still active, and whatever is concluded today may be overturned by the discovery of a new fossil tomorrow. That in some sense is to be hoped for, because only in that way can guesses be falsified and tested as scientific hypotheses.’82

A robust rationale for concluding that the Upper Devonian tetrapods evolved from a fish ancestor, or that they gave rise to Carboniferous tetrapod lineages, is lacking. It is hoped that this paper may stimulate creationists to develop a fuller understanding of these remarkable creatures and their ecological and geological context.83

About the Author

Paul Garner has a B.Sc. (Hons) in Geology and Biology and is a Fellow of the Geological Society of London. He works full-time as a speaker and researcher with Biblical Creation Ministries in the UK. He is also a Committee Member of the Biblical Creation Society, co-editor of the BCS journal, Origins, and is on the Board of The Genesis Agendum, a charitable company promoting church and public awareness of the substantial historical and scientific evidence supporting the biblical record.

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Abstract

Tetrapod fossil tracks are known from the Middle Devonian (Eifelian at ca. 397 million years ago - MYA), and their earliest bony remains from the Upper Devonian (Frasnian at 375–385 MYA). Tetrapods are now generally considered to have colonized land during the Carboniferous (i.e., after 359 MYA), which is considered to be one of the major events in the history of life. Our analysis on tetrapod evolution was performed using molecular data consisting of 13 proteins from 17 species and different paleontological data. The analysis on the molecular data was performed with the program TreeSAAP and the results were analyzed to see if they had implications on the paleontological data collected. The results have shown that tetrapods evolved from marine environments during times of higher oxygen levels. The change in environmental conditions played a major role in their evolution. According to our analysis this evolution occurred at about 397–416 MYA during the Early Devonian unlike previously thought. This idea is supported by various environmental factors such as sea levels and oxygen rate, and biotic factors such as biodiversity of arthropods and coral reefs. The molecular data also strongly supports lungfish as tetrapod's closest living relative.

Citation: George D, Blieck A (2011) Rise of the Earliest Tetrapods: An Early Devonian Origin from Marine Environment. PLoS ONE 6(7): e22136. https://doi.org/10.1371/journal.pone.0022136

Editor: Brock Fenton, University of Western Ontario, Canada

Received: February 7, 2011; Accepted: June 16, 2011; Published: July 14, 2011

Copyright: © 2011 George, Blieck. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The authors have no support or funding to report.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Terrestrialization may be defined as the series of processes (adaptation) that makes an aquatic organism capable of living and sustaining itself on land. It is usually considered as one of the most important events in the evolutionary history of life on Earth. It has occurred several times, that is among primitive organisms (bacteria, protists, fungi…), plants, invertebrates and vertebrates. Here we focus on vertebrate terrestrialization also known as evolution of fish to tetrapods. Lobe-finned fishes (Sarcopterygii) were a highly successful group during the Devonian, between ca. 416 and 359 million years ago (MYA). According to the most recent discoveries and ideas, terrestrialization of vertebrates has occurred in two steps: 1) the first tetrapods diverged from sarcopterygians during the Frasnian (about 375–385 MYA) or earlier in aquatic environments [1], [2], [3]; 2) this was followed by adaptation to terrestrial life much later in the earliest Carboniferous, about 345–359 MYA. Today only three groups of sarcopterygians survive, namely Tetrapoda, Dipnoi (lungfishes), and Actinistia (coelacanths). Tetrapods include about 21,100 extant species and a much greater number of extinct species; only six species of lungfishes and two species of coelacanths exist to-day, but both groups were much more abundant and diverse in the Devonian. It is generally accepted that elpistostegids, a group of extinct sarcopterygian fishes, are the closest relatives (sister-group) of tetrapods [4]. The early vertebrate expert community very often follows the idea originally proposed by A. S. Romer (e.g. [5]) that early tetrapod life occurred in freshwater under the “Drying Pond” scenario where tetrapods evolved from lobe-finned fishes driven onto the land by drought. A modern version of this scenario is that tetrapods evolved from the elpistostegids, probably in brackish to freshwater environments, in response to the modification of their environment [6]. This scenario has however been strongly contradicted as early as the 1950s (refs in [5]) and replaced by the idea that the transition from fish to tetrapod occurred in marine to land/sea transitional environments (tidal, intertidal or lagoonal zones) [7], [8], [9], [10], [11]. Devonian tetrapods and elpistostegids have been found in a wide range of geographic localities, including the Old Red Sandstone Continent, North China, and East Gondwana. This wide range could be due to marine tolerance. The first tetrapods, like their immediate piscine sister taxa, were capable of marine dispersal, thus explaining the widespread global distribution achieved in the Frasnian [12], [13]. The recent discovery of tetrapod tracks from Poland [11] also suggests that the earliest evolution of tetrapods could have taken place in marine to land/sea transitional environments. Study of such relationships between living organisms and environmental conditions at global scale is generally known as geobiology (biosphere-geosphere interactions).

Attempts were made for a long time to determine whether or not sister relationships in the phylogenetic tree of vertebrates exist between tetrapods and lungfishes, tetrapods and coelacanths, or lungfishes and coelacanths. The mitochondrial [14], [15], ribosomal [16], and nuclear [17], [18] encoded sequences have been collected with the specific goal of resolving the relationships among living sarcopterygians, but the available molecular data has not provided complete resolution to whether lungfishes are the closest living relatives to tetrapods, or coelacanths are the closest, or the third case where both coelacanths and lungfishes could be equally related to tetrapods. The proteins used in this analysis on dipnoans, coelacanths and basal tetrapods (amphibians) are the 13 proteins synthesized by the mitochondrial genome. Modifications in the mitochondrial protein coding genes which are involved in oxidative phosphorylation (a process in cell metabolism by which respiratory enzymes in the mitochondria synthesize ATP, which is used to produce energy) can directly influence metabolic performance of an organism. Because of the importance of this biochemical pathway, evaluating selective pressures acting on mtDNA (mitochondrial DNA) proteins could provide key insight into the adaptive evolution of the mtDNA genome. One important goal of the present paper is to compare molecular to paleontological data in order to improve our view of early steps of tetrapod evolution, and place this process into a geobiological approach.

Materials and Methods

The 13 proteins synthesized by the mitochondrial genome of 17 species (see Table S1) were obtained from the NCBI (National Centre for Biotechnology Information). Only 17 sequences were used to avoid noise (convergent evolution) in the genes used, since amphibians seem to have a higher rate of nucleotide substitution while coelacanths and Australian lungfish have a lower rate. This will cause many problems when trying to compute any phylogenetic analysis. All the 12 species of tetrapods used were amphibians (in which 6 were salamanders). It was made sure that representatives from all the 3 orders of Amphibia namely Caudata (salamanders, newts, etc.), Anura (frogs, toads), and Gymnophiona (caecilians) were taken in the analysis. Since there is still debate about the relationship between coelacanths, lungfishes and tetrapods, an exact tree cannot be used for the analysis by TreeSAAP (Selection on Amino Acid Properties using phylogenetic Trees) [19]. Hence the analysis was performed by computing the 12 tetrapod species separately, 3 lungfishes and 2 coelacanths. Physicochemical amino acid changes among residues in mitochondrial protein coding genes were identified by the algorithm implemented in TreeSAAP, which compares the observed distribution of physicochemical changes inferred from a phylogenetic tree with an expected distribution based on the assumption of completely random amino acid replacement expected under the condition of selective neutrality. TreeSAAP also helps us to find positive or negative selection in the given sequences (Positive selection indicates that amino acid replacements are being preferred by natural selection, whereas negative selection means they are less frequent than expected by chance and are influenced by negative or purifying selection). This is done by computing the influence of amino acid properties in the given sequences. The positive selection was calculated by taking two different considerations. In the first consideration the values (called z-scores) of the individual amino acid sites were analyzed, and in the second consideration the entire protein sequence values was analyzed. For the calculation of positive selection when the entire protein was taken into analysis, the total sum value of all the individual amino acid sites needs to be calculated, this included the positive selection and the negative selection values of the individual amino acid sites. For example assume a protein has 4 amino acids. Assume the individual amino acid site values are 2, −2, −6, 4. Hence one amino acid site has been influenced by positive selection (any value above 3.09 was considered as positive selection, this value is most commonly used for this program). Now to calculate the positive selection when the whole protein sequence is taken to consideration add all the values (2+(−2)+(−6)+4 = −2). Since −2<3.09 this protein has not undergone positive selection (the detailed z-scores given by TreeSAAP are available on request to the corresponding author). Hence different results are possible when the entire protein sequence and individual amino acid sites are analyzed. Out of the 31 amino acid properties available in the software, only 20 were used in the analysis (see Text S1). This was done to increase the accuracy in detecting protein adaptation and to prevent false indications of protein adaptation. TreeSAAP was implemented by grouping changes into categories from 1 to 8, 1 being the most conservative and 8 being the most radical. When positive selection is detected in lower, more conservative magnitude ranges (categories 1, 2, or 3), the amino acid properties are considered to be under a type of stabilizing selection (here defined as selection that tends to maintain the overall biochemistry of the protein, despite a rate of change that exceeds the rate expected under conditions of chance). Conversely, when positive selection is detected in greater, more radical magnitude ranges (categories 6, 7, or 8), the amino acid property or properties are considered to be under destabilizing selection (here defined as selection that results in radical structural or functional shifts in local regions of the protein). We make the assumption that positive-destabilizing selection represents the unambiguous signature of molecular adaptation because when radical changes are favored by selection, they result in local directional shifts in biochemical function, structure, or both. For such changes to be favored by selection (i.e., for such changes to be more abundant than expected by chance), they must instill an increased level of survival and/or reproductive success in the individuals who possess and propagate them (refer [20] for more details). In this study we choose to focus on amino acid property changes of categories 6, 7, and 8 because they unambiguously indicate a significant change in the protein (See Table S2).

The GEOCARBSULF model [21] was used to know the atmospheric oxygen levels during the Devonian. It is a combination of earlier GEOCARB models for CO2 and the isotope mass balance model for O2. GEOCARBSULF is a computer model that takes account of the major factors thought to influence atmospheric O2 and CO2. These models account for “forcings,” which are processes that affect the levels of these gases. Principal forcings for O2 are burial of organic matter and pyrite (FeS2) in sediments, their weathering on the continents, and rates of metamorphic and volcanic degassing of reduced carbon and sulfur-containing volcanic gases, such as sulfur dioxide.

Results

Adaptive Evolution Results

Amino acid properties with signals of strong positive selection accumulated at a rate roughly equivalent to the mutation rate of the gene itself (i.e. mutation rate of ATPase (Adenosine Triphosphate Synthase)>ND (Nicotinamide adenine dinucleotide dehydrogenase)>CYTB (Cytochrome b)>COX (Cytochrome c Oxidase)). This correlation is more pronounced for the protein-coding genes with higher mutation rates, such as ATPase and ND, as is most apparent in analyses of the variation. The best correlation between overall mutation rate and number of sites with radical amino acid changes was observed for NDs, while the existence of several outliers for ATPase slightly reduced the strength of the correlation. The biochemical complexity of the oxidative phosphorylation processes precludes a clear discussion on the functional implications of the amino acid properties that are under selection. The amino acid properties under positive destabilizing selection when the entire protein sequence was taken into consideration for analysis are Solvent accessible reduction ratio, Thermodynamic transfer hydrophobicity. This feature was observed only for the amphibians. No positive destabilizing selection was observed when the entire protein sequence of lungfishes and coelacanths were taken into consideration for analysis. But positive destabilizing selection was observed when individual amino acid sites were taken into consideration. Protein sequences in all the three groups namely amphibians, coelacanths and lungfishes (see Table 1) showed positive selection. Individual amino acid sites influenced by positive destabilizing selection were more similar between lungfishes and amphibians (439 similar sites from 13 proteins) than between coelacanths and amphibians (98 similar sites from 13 proteins). The least similarity was found between lungfishes and coelacanths (16 similar sites from 13 proteins). Please note that the values in Table 1 are NOT to be totaled since the table only lists the major properties, and also a same amino acid site might have been affected by more than one amino acid property, hence if values in Table 1 are added it will give an incorrect higher value (Refer Table S2).

Geobiological Data

Most recent interpretations about the origin of tetrapods and their Devonian representatives lead to conclude that they originated before the Middle Devonian, and probably in the Early Devonian [1], [11], [22]. It is here that the trackway found in the courtyard of Glenisla Homestead, in the Grampians Mountains, western Victoria, Australia [22] takes all its importance [1], [23]. Because of its age (see here below under ‘Discussion’) it does indeed bring a physical argument for an Early Devonian origin of tetrapods. So, higher levels of atmospheric oxygen from the GEOCARBSULF model and the revised model [21] that were detected in the Early Devonian at ca. 397–416 MYA seem to coincide with the “elpistostegid-tetrapod changeover” (sensu[11]). Interestingly there seems to be an increase in terrestrial arthropod orders, autotrophic reef biodiversity, marine invertebrate size and genera during the same time [24], [25], [26], [27]. Although coincidence is not necessarily evidence of correlation, it is suggested here that these events were indeed related. Another important finding from the analysis is the re-confirmation of the earliest Carboniferous Romer's Gap as a low oxygen interval [24] although the revised GEOCARBSULF model [21] shows a higher oxygen level than the previous model (Fig. 1). Compared to the Early Devonian genus-level biodiversity of marine invertebrates of about 585 genera, the Early Carboniferous one is below 400 genera [25] which fits with a lower oxygen interval although further analysis would provide better insights and improved clarity to the problem.

Figure 1. Genus-level biodiversity and phylogenetic relationships of elpistostegid fish and earliest tetrapods, as compared to abiotic and biotic features of Devonian environments.

Due to the choosen phylogenetic scheme (after [11]), and the fact that we take into consideration the Glenisla trace fossils from Australia, ghost ranges of basal taxa (elpistostegids, from Panderichthys to Livoniana) and tetrapods (from ANSP 21350 to the crown group ‘Tulerpeton + modern amphibians’) are increased in a significant amount. We use oxygen levels predicted by GEOCARBSULF [21], evolution of arthropod orders [24], evolution of autotrophic reefs [27], body volume of marine invertebrates [26], and genus-level diversity of marine invertebrates [25]. It must be noted that in the highlighted zone of the diagram, the arthropods concerned with are three clades of terrestrial arthropods (myriapods, arachnids, hexapods). Hence the image gives a view of changes in terrestrial and marine species, but giving stress about the changes in marine environment since this is where the tetrapods evolved. The Zachelmie tracks [11] are quite close to the highlighted region and the Glenisla tracks [22] find a satisfactory position amongst the controversy in our image.

https://doi.org/10.1371/journal.pone.0022136.g001

An important point to stress is the influence of the fossil record (likelihood of preservation, differences in paleoenvironments, abundance of field prospectionss, etc.) that certainly has an influence on the observed fossil diversity. Additionally it appears that many paleontologists (including the present senior author) had wrong impressions concerning the fossil diversity through time. A single example is given here, viz. the number of genera of reef builders that is higher in the late Early Devonian than in the rest of the Devonian (Fig. 1). It is indeed often said and tought that the most important period of coral reef development has been the Givetian-Frasnian (late Middle to early Late Devonian) time slice when huge reef systems, compared to the present day Australian Great Barrier, were developed in, e.g., Canadian Arctic or Western Australia [28], [29], [30]. However, most recent global evaluations of reef diversity in the Devonian show that this is not the case, the highest mean reef thickness and reef diversity being reached in the late Early Devonian [27], [31]. Such reappraisal for a single group of organisms, if generalized to all terrestrial and aquatic Paleozoic taxa, will certainly give a very different picture from the classical one depicted by, e.g., the ‘Sepkoski Curve’ ([32], and later critical reevaluations such as, e.g., [25], [33]). This very interesting topic is, however, out of the scope of the present paper.

Discussion

The major amino acid properties affecting the similar regions in the genes of amphibians, lungfishes, and coelacanths (see Table S2) are Equilibrium constant (ionization of COOH), Surrounding hydrophobicity, Power to be at the N-terminal, Solvent accessible reduction ratio, Hydropathy, Compressibility, Mean r.m.s. fluctuation displacement, Thermodynamic transfer hydrophobicity, Polarity. All the above properties were detected as influencing in a positive destabilizing selective direction. Since positive destabilizing selection indicates significant change in the protein, only such changes were taken in account for the analysis. When radical changes are favored by selection, they result in local directional shifts in biochemical function, structure, or both. Increase in Equilibrium constant (ionization of COOH) could influence the efficiency of a protein, interestingly this property would reduce the radical oxygen species production which would increase the longevity of the species since it is generally considered now that increase in radical oxygen species is the main reason for aging [34]. Surrounding hydrophobicity refers to the tendency for the region around the amino acid site in question to interact with water. This is important in our case since the proteins used here are transmembrane proteins. It is similar to hydropathy. The proteins becoming more hydrophobic could mean that many residues get buried inside making the protein more compact. Compressibility is a very important property since it influences the stability of the protein which shows that they have become more stable. Solvent accessible reduction ratio is the property that has mostly affected the proteins. The increase in this value suggests that proteins could have become bulkier and allowing more space for active site formation. The adaptive evolution data shows that Equilibrium constant (ionization of COOH) is the property that has influenced the genes to the second highest extent (Table 1), it drives a more product driven reaction in tetrapod mitochondrial proteins which is why we find a higher value of it affecting the genome.

The levels of oxygen predicted as per GEOCARBSULF [21] has already been studied in relation to tetrapods and arthropods [24]. It is interesting to note that 9 myriapod clades, 4 arachnid clades, and 3 hexapod clades have evolved about 397–416 MYA [24], which seems to confirm the presence of higher levels of oxygen as predicted. Also the increase in distribution of autotrophic reefs [27] could be indicating better formation of reefs in relation to higher levels of oxygen. The diversification of vascular plants [35] and the expansion of high energy predators, including large predatory fish [36], [37], both events of major biological significance, occurred during the same period. An analysis with the use of isotopic composition and concentration of molybdenum in sedimentary rocks [38], and a review of maximum size of organisms through geological time [39] also indicate an increase in oxygen levels in relation to a strong increase in chordate maximum length around 400 MYA. Dahl et al. 's [38] study says that this event could have been the greatest oxygenation (rise in atmospheric oxygen level) event in Earth history.

As concerned with the Glenisla trackway of Australia [22] (G on Fig. 1), it has parallel tracks like some of the Zachelmie tracks of Poland [11]. For some authors (e.g. [40]), the tetrapod interpretation of the Glenisla trackway is very doubtful due to the lack of symmetry of the trackway and the absence of clear alternation in its supposed manus and pes tracks; nevertheless we added it in our Figure 1 because of the possibility that it is of a tetrapod. Even without including the Glenisla trackway in our figure, the radiation of early tetrapods is probably within the Early Devonian after the presently oldest known remains [11] (Z on Fig. 1). Including the Glenisla trackway extends the earliest occurrence of tetrapods near to the base of the Devonian. This has impact on the shape of the elpistostegid-tetrapod cladogram when drawn in front of the geologic time-scale (after [11]), by increasing the ghost range of elpistostegids (a ghost range is an interval of geological time where a fossil lineage should exist, but for which there is no direct evidence) down to the Silurian/Devonian boundary at ca. 416 MYA (Fig. 1). The abundance of oxygen during the Early Devonian could have led to the “elpistostegid-tetrapod changeover”. The higher oxygen levels in the marine environments would have helped the tetrapods to evolve into larger organisms. This could mean that the “changeover” occurred during the arthropod terrestrialization unlike previously thought [24]. The higher oxygen levels suggest that earliest tetrapods never needed to breathe oxygen from the air. This feature might have evolved later when the oxygen levels were lower during the Late Devonian and Early Carboniferous (Fig. 1). In the Silurian, vertebrates (fishes) were generally smaller than in the Early Devonian when larger sizes were developed by both agnathans and jawed fishes, including predatory placoderms and sarcopterygians. The increase in biodiversity (number of genera, Fig. 1) and body size of marine invertebrates suggests almost surely that oxygen levels in the atmosphere and the marine environments did increase during the Early Devonian [26], [27], [38]. So, our hypothesis concerning tetrapods, even if it is highly speculative, does fit more global results on terrestrial and marine biodiversity in general, and in the Devonian in particular.

Another global event occurred in the Early Devonian, that is a relative lowering of sea levels that began in the late Silurian through the late Early Devonian [41]. But the higher oxygen levels means that even shallow marine regions were well oxygenated. These regions could be suitable regions for evolution of tetrapods where “walking” on the bottom or in water would prove useful (see recent results on “walking” chondrichthyans, e.g., [42], [43]); these results let thinking that “walking has evolved many times among different lineages of benthic fishes” (in [43]). Walking is energetically less expensive than swimming and walking is used by thorny skates to capture live prey [43]. Such indications provide more possible reasons for evolution of tetrapods in a shallow marine environment. Generally larger organisms have higher metabolic rates [44] and the increase in efficiency of the proteins could be because the evolution of such species with larger mass can only occur during times of higher oxygen levels.

It may happen in the future that, after revision of the paleobiological databases, the Early Devonian biodiversification event has been as important as the Great Ordovician Biodiversification Event (GOBE: [45], [46]) for Paleozoic life. This is supported by the interpretation of Klug et al. [47] who speak of the Devonian Nekton Revolution (DNR) for the re-organization of marine food webs in the Devonian. The nekton revolution of vertebrates did occur earlier in the Silurian [48], but the elpistostegid-tetrapod transition would participate of the early phase of the DNR and the Predation Revolution of vertebrates [48] at a time of high oxygen level. However, we must keep in mind that such scenarios linking global environmental physical factors (such as the atmospheric and oceanic oxygen rate) with development of life on Earth are a pure practice of uniformitarianism in Earth sciences. “Hypotheses linking evolutionary phenomena to atmospheric oxygen levels can be frustratingly difficult to disprove” [49], and “the fundamentally nonuniformitarian nature of Paleozoic and Proterozoic marine ecology must be taken into account” [50].

Conclusions

Here we suggest that the co-occurrence of a series of bio-events and physical properties of the oceans on Earth during the Early Devonian is not merely a coincidence, but reflects a global re-arrangement of the biosphere. An increase in oxygen is likely to have occurred during the Early Devonian. It would have triggered the emergence of tetrapods in shallow marine environments, where “walking” on the bottom or in the water would have given them advantage in terms of energetic expenses and predation over other fishes. These shallow marine environments could have also proved as ideal regions for the growth of young tetrapods since they could have had fewer predators. We also conclude from the molecular data that lungfishes are much closer to tetrapods than to coelacanths, a result that is not in contradiction with most morphology-based phylogenetic analyses, although it would be hard to pin point and show that these changes shown in the phylogenetic analysis did occur only in the Early Devonian, it is very much a possibility that some of the changes did occur during the Early Devonian. Scenarios such as the ones described above [38], [39], [45], [46], [47] are attractive and represent possible solutions to the relation of global environmental factors and the development of life on Earth. This conclusion is applicable to most, if not all, geobiological scenarios through Earth's history [48].

Acknowledgments

DG would like to thank Kate Jackson (Whitman College, Walla Walla, WA, USA) for inspiring him to do this study. He thanks Jebakumar, Pavan Kumar Singh and Senthil Kumar for the constant motivation; Yuichiro Suzuki (Wellesley College, Wellesley, MA, USA) and Antony Caesar (St Peter's College, Chennai, India) for providing him with key references and comments; Vinoth Kumar, Valivittan, David McClellan, Per Ahlberg, Alice Clement, Matt Friedman, Michael Coates, Mikolaj Zapalski, Michael Joachimski, John Speakman and David Wake for generously providing their papers and/or giving helpful comments to make this paper. He would also like to thank Hans-Peter Schultze (University of Kansas, Lawrence, KS, USA) for providing references and comments; Philip M. Novack-Gottshall (University of West Georgia, Carrollton, Georgia, USA) and Arnaud Bignon (Université Lille 1, Villeneuve d'Ascq, France) for reviewing an earlier version of the paper; and both referees of PLoS ONE for their precise and detailed reviews.

Author Contributions

Conceived and designed the experiments: DG. Performed the experiments: DG. Analyzed the data: DG AB. Wrote the paper: DG AB.

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