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Ever Since Owen: Changing Perspectives on the Early Evolution of Tetrapods

December 2008
Annual Review of Ecology Evolution and Systematics 39(1):571-592

December 2008
39(1):571-592

DOI:10.1146/annurev.ecolsys.38.091206.095546

Authors:

Michael I Coates

University of Chicago

Marcello Ruta

University of Bristol

Matt Friedman

University of Michigan

The traditional notion of a gap between fishes and amphibians has been closed by a wealth of fish-like fossil tetrapods, many discovered since the mid 1980s. This review summarizes these discoveries and explores their significance relative to changing ideas about early tetrapod phylogeny, biogeography, and ecology. Research emphasis can now shift to broader-based questions, including the whole of the early tetrapod radiation, from the divergence from other lobed-finned fishes to the origins of modern amphibians and amniotes. The fish-to-tetrapod morphological transition occurred within the Upper Devonian; the divergence of modern tetrapod groups is all Early Carboniferous event. Modern tetrapods emerged in the aftermath of one of the five major extinction episodes in the fossil record, but the earlier Devonian tetrapod radiation is not well understood. Tetrapod limbs, paired fins, and comparative developmental data are reviewed; again, research emphasis needs to change to explore the origins of tetrapod diversity,

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ANRV360-ES39-27 ARI 10 October 2008 10:36

Ever Since Owen: Changing

Perspectives on the Early

Evolution of Tetrapods

Michael I. Coates,1,2Marcello Ruta,3

and Matt Friedman2

1Department of Organismal Biology and Anatomy, and 2Committee on Evolutionary Biology,

University of Chicago, Chicago, Illinois 60637; email: mcoates@uchicago.edu

3Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road,

Bristol BS8 1RJ, United Kingdom

Annu. Rev. Ecol. Evol. Syst. 2008. 39:571–92

First published online as a Review in Advance on

September 10, 2008

The Annual Review of Ecology, Evolution, and

Systematics is online at ecolsys.annualreviews.org

This article’s doi:

10.1146/annurev.ecolsys.38.091206.095546

2008 by Annual Reviews.

1543-592X/08/1201-0571$20.00

Key Words

phyologeny, development, paleontology, vertebrates, limbs

Abstract

The traditional notion of a gap between ﬁshes and amphibians has been

closed by a wealth of ﬁsh-like fossil tetrapods, many discovered since the

mid 1980s. This review summarizes these discoveries and explores their

signiﬁcance relative to changing ideas about early tetrapod phylogeny, bio-

geography, and ecology. Research emphasis can now shift to broader-based

questions, including the whole of the early tetrapod radiation, from the

divergence from other lobed-ﬁnned ﬁshes to the origins of modern amphib-

ians and amniotes. The ﬁsh-to-tetrapod morphological transition occurred

within the Upper Devonian; the divergence of modern tetrapod groups is an

Early Carboniferous event. Modern tetrapods emerged in the aftermath of

one of the ﬁve major extinction episodes in the fossil record, but the earlier

Devonian tetrapod radiation is not well understood. Tetrapod limbs, paired

ﬁns, and comparative developmental data are reviewed; again, research em-

phasis needs to change to explore the origins of tetrapod diversity.

571

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INTRODUCTION

Archegosaurus (Goldfuss 1847) was the original missing link. Seized by evolutionists after Richard

Owen (1859, in Desmond 1982) declared that this “old Carboniferous reptile” conducted the

march of development from ﬁsh to primitive amphibian, the treatment of Archegosaurus foreshad-

owed portrayals of Ichthyostega,Acanthostega,Tiktaalik, and others besides: each depicted at pond-

or swamp-side with tail trailing (signiﬁcantly) in the water (Milner et al. 1986). Evolutionary trees

of tetrapod ancestry have long since branched and ﬁlled to accommodate earlier and more thor-

oughly transitional forms (Clack 2002), but the vignette of beached missing links has persisted.

Unfortunately, this paleo-clich´

e reduces the exploration of tetrapod origins to the discovery of

substitute candidates for this brief episode in vertebrate history. However, questions about the ori-

gin of tetrapods now concern a much wider range of paleobiological issues. The origin of tetrapods

includes the whole of the tetrapod stem (see sidebar, Deﬁning a Tetrapod), with many groups of

ﬁsh-like (i.e., ﬁnned) taxa only recently being incorporated into this wider framework (Ahlberg &

Johanson 1998, Coates et al. 2002, Jeffery 2002, Johanson et al. 2003). It is now possible to ask

how the origins of the tetrapod total and crown groups relate to morphological changes and the

emergence of a conventional tetrapod body plan. The ﬁn-to-limb transition is an exceptionally

rich area of integrative research and debate (e.g., Z´

ak´

any et al. 1997, Coates et al. 2002, Davis

et al. 2004a,b, Friedman et al. 2007). The origin of tetrapods and the water-to-land transition are

not synonymous, but both events are associated with global climatic, atmospheric, and tectonic

changes, as well as with serial extinctions at the end of the Devonian (Algeo et al. 2001, Berner

et al. 2007, Blieck et al. 2007, Clack 2007). Taxon and character sets are now large enough to

be mined for large-scale evolutionary trends (Ruta et al. 2006, Wagner et al. 2006). This review

gathers reports and articles on this topic published in the past few years—some of which have

gained exceptionally widespread attention—and places them in context and suggests agendas for

future research.

THE POSITION OF TETRAPODS WITHIN VERTEBRATE PHYLOGENY

The ﬁrst question about tetrapod origin concerns the identity of the closest relatives of land

vertebrates. This issue emerged within the nineteenth century (Desmond 1982) as discoveries

of lungﬁshes confounded diagnoses of living tetrapods as a natural group, and after fossil “rhi-

pidistian” ﬁshes were recognized as belonging within the same group as limb-bearing tetrapods.

Widespread acceptance of evolutionary theory redirected systematic research to discover the

particular rhipidistian ancestors of tetrapods. By the early twentieth century, phylogenetic

DEFINING A TETRAPOD

Questions associated with tetrapod origins depend on how a tetrapod is deﬁned. Essentialist, character-based

deﬁnitions create problems because much of the research program concerning tetrapod origins aims to provide

a sequence of intermediates showing the assembly of the anatomical characters in question. Moreover, there is a

built-in presupposition that any deﬁning character has evolved only once. In this review, we adopt phylogenetic

deﬁnitions of groups. Total-group tetrapods include all those taxa more closely related to living tetrapods than to

their nearest living sister group (lungﬁshes), whereas crown-group tetrapods consist of the last common ancestor

of all living tetrapods plus all the fossil and living descendants of that ancestor. Stem-group tetrapods form a

paraphyletic assemblage equivalent to the total group minus the crown group.

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hypotheses had multiplied considerably, and ranged from polyphyletic origins of limbed ver-

tebrates from several rhipidistian groups ( Jarvik 1980; S¨

ave-S¨

oderbergh 1932, and references

therein) to a monophyletic origin from “osteolepiforms” (Watson 1920; also reviewed by Panchen

& Smithson 1987). Rare objections to this rhipidistian hegemony (e.g., Kesteven 1950) were side-

lined. With tetrapod ancestry anchored to speciﬁc fossils, such as the osteolepiform Eusthenopteron,

research focused on the adaptive circumstances surrounding the invasion of dry land.

However, by the late 1970s, this passive acceptance of osteolepiforms as the closest ﬁsh rel-

atives of terrestrial vertebrates provoked a reexamination of the status quo. A withering critique

of research on tetrapod origins (Rosen et al. 1981) concluded that most characters claimed to

link Eusthenopteron to tetrapods were either primitive or spurious. Emphasis was placed on the

choana, a palatal nostril framed by a diagnostic bone arrangement, present in Eusthenopteron and

tetrapods. Lungﬁshes also possess a palatal nostril, homologized by several nineteenth-century

anatomists with the tetrapod choana (Desmond 1982), but dismissed by most twentieth-century

paleontologists as convergent. However, newly prepared material of a Late Devonian lungﬁsh

(Griphognathus) revealed a bone-surrounded palatal nostril that Rosen et al. (1981) offered as

evidence that a true choana was, in fact, present in primitive lungﬁshes.

The ensuing controversy spurred paleontologists to frame explicitly cladistic hypotheses to

refute the arguments of Rosen et al. (1981) and reinstate osteolepiforms as the closest relatives of

limbed tetrapods (e.g., Panchen & Smithson 1987, Schultze 1991). Further evidence emerged from

the discovery of the Early Devonian Diabolepis (Chang 1995, and references therein), combining

lungﬁsh specializations with generalized sarcopterygian conditions, including possession of two

external nostrils. As the sister group of lungﬁshes (Chang 1995), Diabolepis indicates that lungﬁsh

palatal nostrils are convergent with the choanae of limbed vertebrates and osteolepiforms. Two

decades later, another Chinese Devonian ﬁsh, the primitive osteolepiform Kenichthys, added a

postscript to the choana debate: its posterior nostril penetrates the skull exterior close to the

upper jaw rim, presenting a possible incipient condition for the choana (Zhu & Ahlberg 2004). A

summary of the present consensus on sarcopterygian interrelationships is shown in Figure 1 (for

further discussion see Friedman 2007).

DEVONIAN TETRAPOD DIVERSITY

Four major Devonian groups belong to the tetrapod stem lineage: rhizodonts, osteolepidids, tris-

tichopterids, and “elpistostegalids” plus limbed tetrapods (Figures 1 and 2a). Most stem tetrapods

are osteolepiforms, a grade of ﬁn-bearing groups including rhizodonts, osteolepidids, and tristi-

chopterids, but excluding elpistostegalids. Devonian examples are known from every continent

and their diversity totals approximately 40 genera. Devonian tetrapods for which limbs have been

discovered or implied total approximately a dozen genera, although digit-bearing limbs are known

in only three: Acanthostega,Ichthyostega, and Tulerpeton. Approximately seven more unnamed forms

are reported from fragments (Clack 2005). Elpistostegalids are the most informative taxa for un-

derstanding anatomical changes associated with the ﬁsh-to-tetrapod transition. They are known

from a handful of genera, all exclusive to the Northern Hemisphere (Daeschler et al. 2006).

Reliance upon Eusthenopteron in studies of tetrapod origins gives the false impression that few

ﬁn-bearing tetrapods are known. In fact, many are described in detail (e.g., Fox et al. 1995; Lebedev

1995; Long et al. 1997, 2006), but uncertainty about osteolepiform interrelationships obstructs

deeper understanding of tetrapod origins. Rhizodonts and tristichopterids are widely recognized

as clades (Ahlberg & Johanson 1998), but few cladistic analyses have examined this area of tetrapod

phylogeny ( Johanson & Ahlberg 2001, Zhu & Ahlberg 2004). These cladograms place Kenichthys,

from the Eifelian of China, at the base of the tetrapod stem group, followed by (in increasing

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Tetrapod stem

Lissamphibian

total group

Amniote

total group

Outgroup lobe-

ﬁnned ﬁsh clades

Limb-bearing tetrapods

Tetrapod crown node

Panderichthys

Elpistostege

Tiktaalik

Elginerpeton

Ventastega

Acanthostega

Ichthyostega

Tulerpeton

Colosteidae

Crassigyrinus

Whatcheeriidae

Baphetidae

Embolomeri

Gephyrostegidae

Seymouriamorpha

Diadectomorpha

Crown-group Amniota

Microsauria

Lysorophia

Adelospondyli

Nectridea

Aistopoda

Gyroptychius

Tristichopteridae

Temnospondyli

Total-group Actinistia

Total-group Dipnoi

Kenichthys

MEG EK

Rhizodontida

Gogonasus

Osteolepis

Megalichthyidae

Crown-group Lissamphibia

Osteolepiformes

TriassicPermian

Carboniferous

Devonian

LM UMiss Penn Cis Gd Lo LM

416

398

385

359

318

299

271

260

251

245

228

574 Coates ·Ruta ·Friedman

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ANRV360-ES39-27 ARI 10 October 2008 10:36

Devonian tetrapods Carboniferous tetrapods

123

15 16

13 14 15

1 m

Figure 2

(a) Devonian tetrapods drawn to scale, illustrating anatomical diversity; all taxa are stem members. 1. Gooloogongia, a rhizodont;

2. Osteolepis, an osteolepidid; 3. Koharalepis, an osteolepidid; 4. Canowindra, an osteolepidid; 5. Eusthenopteron, a tristichopterid;

6. Tristichopterus, a tristichopterid; 7. Gyroptychius agassizi, an osteolepidid; 8. Gyroptychius dolichotatus, an osteolepidid;

9. Cabonnichthys, a tristichopterid; 10. Mandageria, a tristichopterid; 11. Eusthenodon, a tristichopterid; 12. Glyptopomus, an osteolepidid;

13. Tiktaalik, an elpistostegalid; 14. Panderichthys, an elpistostegalid; 15. Ichthyostega, a limbed stem tetrapod;

16. Acanthostega, a limbed stem tetrapod. (b) Carboniferous tetrapods drawn to scale, illustrating anatomical diversity. Taxa shown

include stem (1–5, 9, 11) and crown group (6–8, 10, 12–15) members. 1. Strepsodus, a rhizodont; 2. Megalichthys, a megalichthyid;

3. Rhizodopsis, a megalichthyid; 4. Megalocephalus, a baphetid (stem tetrapod); 5. Crassigyrinus, a stem tetrapod; 6. Palaeomolgophis,an

adelospondyl (stem amniote or stem tetrapod); 7. Brachydectes, a lysorophid (stem amniote); 8. Urocordylus, a nectridean (stem amniote);

9. Greererpeton, a colosteid (stem tetrapod); 10. Proterogyrinus, an embolomere (stem amniote); 11. Pederpes, a whatcheeriid (stem

tetrapod); 12. Westlothiana, a stem amniote; 13. Silvanerpeton, an embolomere (stem amniote); 14. Dendrerpeton, a temnospondyl (stem

lissamphibian); 15. Gephyrostegus, a gephyrostegid (stem amniote).

proximity to the crown) rhizodonts, a paraphyletic assemblage of osteolepidids, tristichopterids,

and the clade uniting elpistostegalids and limbed tetrapods. One solution places the osteolepidid

Gogonasus crownward of Eusthenopteron (Long et al. 2006), but this topology emerges from a limited

taxon set (Friedman et al. 2007).

The specialized rhizodonts (Figure 2a:1;Figure 2b: 1) branch furthest from the tetrapod

crown node. Rhizodont pectoral ﬁns (see below, The Origin of Tetrapod Limbs: Morphological

Novelty) are characteristic, and have featured in debates about tetrapod limb origin (Davis et al.

2004a), although many limb-related similarities are probably homoplastic (Coates et al. 2002,

Friedman et al. 2007). Few Devonian rhizodonts are known: Aztecia,Gooloogongia,Sauripterus

( Johanson & Ahlberg 2001). The Frasnian Gooloogongia ( Johanson & Ahlberg 2001) is proba-

bly the most plesiomorphic rhizodont known, but it already exhibits most of the clade-speciﬁc

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−

Figure 1

Evolutionary tree of early tetrapods, showing total group with taxon ranges, stem and crown taxa, and the distribution of limb-bearing

(quadrupedal) clades. Important fossil localities are listed above the geological column (M: Miguasha, Quebec, Canada; EG: East

Greenland; EK: East Kirkton, Scotland; J: Joggins, Nova Scotia, Canada). The interrelationships of ﬁnned tetrapods are adapted from

Ahlberg & Johanson (1998), whereas those of limbed tetrapods are adapted from Ruta et al. (2003).

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Eusthenopteron

(osteolepiform)

Panderichthys

(elpistostegalid)

Acanthostega

(limb-bearing tetrapod)

Braincase

Hyoid arch

Gill arches

Vertebral

column

Primary

(endoskeletal)

pectoral

girdle

Primary

(endoskeletal)

pectoral ﬁn/

forelimb

Finweb

(dermal

skeletal)

Figure 3

Eusthenopteron (top), Panderichthys (middle), and Acanthostega (bottom), shown in lateral aspect. Anatomical

systems are color-coded. Light-shaded components of visceral skeleton in Panderichthys are inferential.

specializations. Carboniferous rhizodonts achieved colossal sizes; at an estimated length of seven

meters ( Jeffery 2002), Rhizodus was probably the largest Paleozoic osteichthyan.

Osteolepidids (Figure 2a: 2–4, 7, 8, 12; Figure 2b: 2, 3) lie crownward of rhizodonts and

include many generalized stem-group tetrapods. They are probably paraphyletic and their in-

terrelationships remain uncertain. Megalichthyids probably constitute a legitimate clade within

osteolepidids. Persisting in continental settings into the Permian, megalichthyids (Figure 2b:2,3)

were the last ﬁn-bearing stem tetrapods.

The superﬁcially pike-like tristichopterids are placed crownward of osteolepidids (Figure 2a:

5, 6, 9, 11). Eusthenopteron is the best-known genus (Figure 3), a modestly sized (80 cm) repre-

sentative that features repeatedly in debates about tetrapod origins. Tristichopterids range from

the Givetian to the Famennian, and trend toward increasing body size. The phylogenetically most

basal and earliest form, Tristichopterus, was approximately 30 cm long, whereas apical members of

this clade exceeded several meters in length (Figure 2a: 10, 11; Ahlberg & Johanson 1997). Like

576 Coates ·Ruta ·Friedman

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ANRV360-ES39-27 ARI 10 October 2008 10:36

rhizodonts, derived tristichopterids display elongated bodies and reduced median ﬁns (Figure 2a:

10), suggesting convergence upon similar ecological roles (Ahlberg & Johanson 1998).

Elpistostegalids (Figure 2a: 13, 14) are the closest ﬁsh-like relatives of limbed tetrapods and

form another paraphyletic grade. Synapomorphies with limb-bearing tetrapods include a ﬂattened

skull with dorsal orbits, a sutured dermal intracranial joint, paired frontal bones, an enlarged en-

doskeletal shoulder girdle, and absence of dorsal and anal ﬁns (Ahlberg et al. 1996, Daeschler

et al. 2006, Vorobyeva & Schultze 1991). Three elpistostegalids are known in detail: Panderichthys,

Elpistostege, and Tiktaalik. Two others, Livoniana and Parapanderichthys, are known only from frag-

ments (Ahlberg et al. 2000). The Frasnian Tiktaalik and Elpistostege appear more closely related

to limbed tetrapods than do the Givetian Panderichthys (Daeschler et al. 2006). Notably, Elpis-

tostege was presented as a limb-bearing tetrapod (Westoll 1938) long before detailed accounts of

Panderichthys were published.

Resurgent research into tetrapod origins over the past two decades has been most apparent in

the ﬁeld of limb-bearing Devonian forms (Figure 2a: 15, 16). When Rosen et al. (1981) appeared

on the scene, Ichthyostega (S¨

ave-S¨

oderbergh 1932) was the only Devonian tetrapod known to have

limbs. A detailed redescription of this taxon took over 60 years to appear ( Jarvik 1952, 1980, 1996).

Acanthostega was known only from two incomplete skulls ( Jarvik 1952), whereas Metaxygnathus,

an eroded jaw from Australia, was claimed to belong to a limb-bearing tetrapod (Campbell &

Bell 1977). Tulerpeton was the ﬁrst Devonian newcomer to emerge, reported on the basis of an

articulated trunk bearing hind- and forelimbs, the latter of which bore six digits (Lebedev & Coates

1995). It remains on the fringes of the tetrapod origins debate because its advanced characteristics

resemble post-Devonian forms.

The revolution in understanding the morphological transformation from ﬁn-bearing to limb-

bearing tetrapods began with renewed expeditions to East Greenland that recovered complete

specimens of Acanthostega (Clack 2002). This material revealed an animal less than a meter in

length with a series of characters betraying its aquatic habit: a well-developed gill skeleton [Coates

& Clack 1991; a gill skeleton has subsequently been reported in Ichthyostega (Clack et al. 2003)],

paddle-like limbs bearing eight digits each (Coates 1996), and a tail with ﬁn rays and radials (Coates

1996). These ﬁnds challenged the established notion that limbs evolved for terrestrial locomotion,

and instead placed their origin squarely within an aquatic environment.

Acanthostega also yielded a series of jaw characters unique to limbed tetrapods. The resultant

rash of new taxa based on isolated mandibles and mandible fragments has expanded the nominal di-

versity of Devonian forms and provided useful stratigraphic and geographic markers [Elginerpeton

(Ahlberg 1991); Ventastega (Ahlberg et al. 1994); Obruchevichthys,Densignathus (Clack 2002); Sinos-

tega (Zhu et al. 2002); unnamed Belgian “ichthyostegid” (Clement et al. 2004)]. However, although

these fragmentary taxa are conventionally described as tetrapods (in the sense of limb-bearing ver-

tebrates rather than the total-group deﬁnition applied here), digit-bearing limbs have not been

recovered for any of them. Ventastega (Ahlberg et al. 1994, 2008) and Elginerpeton (Ahlberg 1991,

1998) each have a suite of attributed nonmandibular material. However, uncertainty surrounds the

identity of some of the Elginerpeton material, most notably the putative humerus (Ahlberg 2004,

Coates et al. 2004).

CARBONIFEROUS TETRAPOD DIVERSITY

Irrespective of ﬁnned or limbed conditions, tetrapod diversity in the earliest part of the Early

Carboniferous is poor (Figure 1); it is unclear whether this reﬂects impoverished faunas or simply

a lack of available facies. This period, often referred to as Romer’s gap, occupies much of the

Tournaisian, about 360 to 350 mya. Limbed tetrapods from the upper part of the Tournaisian

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(about 350 to 345 mya) are known only from the nearly complete skeleton of a whatcheeriid,

Pederpes, from Scotland (Clack & Finney 2005), and fragments, mostly postcranial, from the

slightly older locality at Horton Bluff, Nova Scotia (Clack 2002). Pederpes approached a meter

in length (Figure 2b: 11), and, like other whatcheeriids, had a robust skull and a well-ossiﬁed

postcranial skeleton with stout limbs bearing at least ﬁve digits, probably the earliest examples

suited for terrestrial walking (Clack & Finney 2005). Further remains of similarly sized and larger

whatcheeriids include Ossinodus from the mid-Vis´

ean of Australia (Warren 2007) and Whatcheeria

from a cache of spectacularly well-preserved skeletons from the upper Vis´

ean of Iowa, United

States (Bolt & Lombard 2000).

Unlike the limited record of Tournaisian tetrapods, the diversity of Vis´

ean tetrapods is spectac-

ular and Scottish sites deliver remarkable evidence of the diversiﬁcation of crownward taxa. From

Gilmerton (mid-Vis´

ean) comes the holotype of the large (nearly two meters in length), grotesque,

and Moray eel-like stem tetrapod, Crassigyrinus (Clack 2001) (Figure 2b: 5). The deep-sided skull

resembles those of watcheeriids, but the axial skeleton is meager and the appendicular skeleton

highly reduced. Gilmerton has delivered two further large tetrapods, a baphetid and a colosteid

(Clack 2002). Both examples are the earliest occurrences of their respective clades. Baphetid skulls

are large (250 mm+in length) and many are superﬁcially crocodile-like (Figure 2b: 4), although

with anteriorly extended orbits; their postcranial anatomy is mostly unknown. Colosteids are one

of the more widely represented and well-preserved groups of early, limb-bearing stem tetrapods.

More than a meter in length and with ﬂattened skulls and postcrania, colosteids (Figure 2b:9)

resemble long-trunked giant salamanders (Godfrey 1989) and, correspondingly, are interpreted

as mostly aquatic.

Unlike these bulky Gilmerton tetrapods, from Cheese Bay (also mid-Vis´

ean) originates the

gracile, small (hip to shoulder length: 80 mm) but headless specimen of Casineria (Paton et al.

1999). This extraordinary fossil echoes the signal from Tulerpeton, displaying postcranial skeletal

anatomy far advanced beyond those of its known contemporaries, and in this instance exhibiting

characteristics of taxa close to the amniote crown.

Lethiscus (Anderson et al. 2003) from the mid-Vis´

ean Wardie Shales of Scotland reveals a further

new aspect of tetrapod diversity: secondary limb-loss. Lethiscus is the earliest of the a¨

ıstopods:

snake-like with 80+vertebrae; no trace of limbs and girdles; and, like Casineria, of small size (skull

length: 60 mm).

Adelospondyls (Andrews & Carroll 1991) represent a further clade of small (total length: 300

mm), secondarily limbless tetrapods (Figure 2b: 6) that, unlike a¨

ıstopods, retained their pectoral

girdle and were probably largely aquatic. Known from several sites of similar age to Cheese Bay

and Gilmerton and extending through to the Serpukhovian, adelospondyls are among the most

abundant tetrapods in the early to mid-Carboniferous beds of Scotland (Milner et al. 1986).

A¨

ıstopods and adelospondyls are two subgroups of a much larger grade or clade, the lep-

ospondyls. Often compared with small lizards and snakes, lepospondyls are characterized by pos-

session of spool-shaped centra. Miniaturization probably underlies many of the apparent spe-

cializations manifest in this group. Other lepospondyl clades include the microsaurs, nectrideans

(Figure 2b: 8), lysorophids (Figure 2b: 7), and acherontiscids. The challenge of summarizing

lepospondyls within the conﬁnes of a short article underscores their remarkable morphological

diversity (Anderson 2001, Clack 2002, Ruta et al. 2003). Temporal ranges of all member clades

are conﬁned to the Carboniferous and Permian (Milner 1993) (Figure 1).

Temnospondyls constitute a second, temporally long-ranging tetrapod group that appear ﬁrst

within the Early Carboniferous. But, unlike lepospondyls, temnospondyls persist well into the

Mesozoic (Milner 1993). Temnospondyl adult size ranges vary from a few centimeters to an

estimated seven meters or more. Approximately salamander-like (although evolving into a vast

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range of body shapes and sizes, presumably with attendant variation in life habits), temnospondyls

exhibit usually broad and ﬂat skulls with wide openings in the palate; the axial skeleton bears short

ribs (except in large forms) and forelimbs have four digits (Figure 2b: 14). Temnospondyls have

long been associated with amphibian ancestry and include the already mentioned Archegosaurus

(Clack 2002, Milner 1993).

Anthracosaurs are a third group commonly encountered in descriptions of early tetrapod di-

versity; once again, these have uncertain monophyletic status. Anthracosaurs also appear ﬁrst in

the Early Carboniferous. They radiate throughout the remainder of the Paleozoic, and range

from small- and medium-sized terrestrial forms (Figure 2b: 10, 13) to large predatory aquatic

genera (embolomeres, another group compared to modern crocodiles) that infested Late Car-

boniferous coal swamps (Clack 2002, Holmes 1984). Putative anthracosaur synapomorphies have

frequently emerged as no more than persistent symplesiomorphies. Although long associated with

the amniote stem, this link appears to be increasingly tenuous.

The late Vis´

ean locality of East Kirkton, Scotland, is probably the most renowned site for

Early Carboniferous tetrapods. This fossil biota is diverse (Clarkson et al. 1994) and opens a

unique window on the earliest known terrestrial vertebrate community (Ruta & Clack 2006).

East Kirkton tetrapods include a baphetid (Clack 2001), anthracosaurs (Clack 1994, Ruta &

Clack 2006, Smithson 1994), and the superﬁcially lizard-like Westlothiana (Smithson et al. 1994)

(Figure 2b: 12). East Kirkton lepospondyls include an undescribed microsaur ( J. Clack, work in

progress) and an a¨

ıstopod (Milner 1994). Temnospondyls are present, including small and large

examples (Milner & Sequeira 1994). It is noteworthy that, like Lethiscus and Casineria, these early

terrestrial tetrapods are generally small (approximately 300 mm in total length).

Many tetrapod sites are known throughout the remainder of the Carboniferous. Signiﬁcant ex-

amples include Greer in West Virginia (mid-Carboniferous) and the numerous classic faunas from

coal swamps and deltaic fans of the Pennsylvanian of Illinois (Mazon Creek), Ohio (Linton), Nova

Scotia ( Joggins), Ireland ( Jarrow), England (Trawden, Newsham), and Slovakia (Nyrany) (Clack

2002, Milner et al. 1986). Unlike East Kirkton, all of these faunas have a distinctly semiaquatic

signature. The Joggins locality deserves particular mention because of its historical and biotic

signiﬁcance. Dating from the mid-Bashkirian (Ryan et al. 1991), the Joggins fauna includes one of

the most primitive known temnospondyls, Dendrerpeton, as well as the earliest widely agreed-on

crown group amniote, Hylonomus (Clack 2002), a marker used repeatedly in molecular estimates

of vertebrate evolutionary history.

TREE SHAPES, NODE DATES, AND THE ORIGIN

OF CROWN-GROUP TETRAPODS

Phylogenies of early limbed tetrapods obtained from analyses of large taxon and character sets

ﬁrst appeared in the mid-1990s (Carroll 1995, Laurin & Reisz 1997). Subsequent analyses (e.g.,

Laurin & Reisz 1999, Vallin & Laurin 2004) have indicated that the majority of Carboniferous

tetrapods are members of the stem group. In these trees, the earliest crown-group tetrapods are

the morphologically diverse lepospondyls, and these branch from the amphibian stem. In contrast,

the amniote stem is represented solely by diadectomorphs: bulky, stout-limbed tetrapods that ﬁrst

appear in the Moscovian. More recent analyses have presented a somewhat different phylogenetic

structure (Ruta & Coates 2007, Ruta et al. 2003) in which most Carboniferous limbed tetrapods

are included within the crown. The amphibian stem is populated by temnospondyls, whereas the

lepospondyls branch from the amniote stem, along with the anthracosaurs (as shown in Figure 1).

This branching pattern conforms more closely to previous ideas about the afﬁnities of early

tetrapods to amphibian and amniote lineages (cf. Milner et al. 1986).

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Importantly, under either phylogenetic regime, the a¨

ıstopod lepospondyl Lethiscus is the ear-

liest crown-group tetrapod, dating the amphibian-amniote divergence to a minimum of around

335 mya. The equivalent fossil marker for the divergence of lungﬁshes and tetrapods (Diabolepis)

lies close the base of the Devonian, suggesting that the temporal span of the tetrapod stem group

exceeds 50 million years (but note that this time range lacks hard boundaries).

It is also signiﬁcant that both sets of phylogenies exclude all known Devonian limbed tetrapods

from the tetrapod crown; post-Devonian limbed tetrapods are monophyletic relative to earlier

members of the clade. Acanthostega,Ichthyostega, elpistostegalids, and fragments of putative near-

relatives have not yet turned up in post-Devonian deposits. The suggestion that Tulerpeton might

represent a basal “reptiliomorph” (stem amniote) (Lebedev & Coates 1995) has not survived

subsequent analyses (Ruta & Coates 2007, Vallin & Laurin 2004). However, an isolated humerus

from the early Carboniferous of Horton Bluff seems to link the humeri of Tulerpeton and early

anthracosaurs (Ruta & Clack 2006), whereas another study (Ruta & Bolt 2006) groups Tulerpeton

with Carboniferous whatcheeriids.

Irrespective of these tenuous connections across the Devono-Carboniferous boundary, the

topology of tetrapod phylogeny shows post-Devonian limbed tetrapods as products of a phylo-

genetic bottleneck (sensu Jablonski 2002), yielding a second radiation into semiaquatic ecospace.

Subsequently, by the mid-Vis´

ean, groups of limbed tetrapods had established divergent character

complexes and, by extension, different life habits. These and many other distinguishing features

persist, in certain respects remarkably unchanged, into the later evolutionary history of the am-

phibian and amniote stem groups.

Evolutionary radiations are often marked by rapid diversiﬁcation of new morphotypes

(Wagner 2001), and tetrapods provide an increasingly well-deﬁned example in which the origin

of a new body-plan is associated with invasion of new habitat, as well as origin of a crown-group

radiation. Given this context, the pattern of tetrapod phylogeny might allow for comparison be-

tween contrasting models for reducing rates of morphological change (Valentine 1980): either

intrinsic constraint (i.e., developmental or genetic) or ecological restriction (i.e., ﬁlling of general

ecospace). In fact, limbed tetrapods displayed a dramatic decrease in amounts of evolutionary

change between the Devonian and the Early Carboniferous (Ruta et al. 2006). The initial peak

of morphological evolution could easily represent relaxation of both kinds of constraint: reduced

ecological restrictions and reduced intrinsic developmental and/or genetic constraints. Decreased

rates of morphological evolution in the Early Carboniferous present a marked contrast, and these

are associated with an apparent repeated radiation into marginal terrestrial habitats. If ecology

alone were responsible for rates of morphological change, then Early Carboniferous rates ought

to mimic Devonian rates. It follows that the very marked drop in rate change could be a result of

increased intrinsic constraint. However, this assumes a simple model of empty or cleared ecospace,

whereas, at present, we have very limited knowledge of the Early Carboniferous ecosystems that

stem tetrapods occupied.

TRANSFORMATIONS: THE EMERGENCE OF A NEW BODY-PLAN

Most anatomical changes associated with the origin of limbed tetrapods occurred in groups en-

compassing the upper reaches of the tetrapod stem (Figure 1). Figure 2 illustrates large-scale

changes to body proportions and external features, such as ﬁns and opercular ﬂaps. Figure 3 details

the forequarters of three genera that have come to epitomize the ﬁsh-to-tetrapod morphological

transition: Eusthenopteron,Panderichthys, and Acanthostega.

Within the skull, the braincase (neurocranium)—primitively separated into anterior and poste-

rior divisions—unites, and proportions change so that the anterior portion is much longer than the

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rear portion. The auditory capsules increase in size relative to the posterior division of the brain-

case, and the notochord is withdrawn from a tunnel beneath the braincase rear. These changes

are reﬂected in transformation of the overall skull morphology, including snout enlargement and

shifts in orbit position and orientation.

The gill skeleton (viscerocranium) is reduced, but ossiﬁed arches with deep grooves persist in

the earliest limbed tetrapods. The hyoid arch is transformed as the palate (not shown) becomes

attached securely to the braincase. The lower division of the hyoid arch, the ceratohyal, remains

large and probably retained primitive functions associated with jaw, gill arch, and oropharyngeal

volume change. The upper division, the hyomandibula, is reduced and reoriented as a primitive

stapes. Instead of articulating wholly with the ossiﬁed sidewall of the auditory capsule, the proximal

end of the nascent stapes sits mostly within an unossiﬁed window. No longer associated clearly with

jaw suspension, the hyomandibula/stapes might have had an incipient role in sound conduction

and/or spiracular pouch function (Clack 2002, 2007).

Postcranially, the persistently notochordal vertebral column gains expanded centra and upright

neural spines, while ribs enlarge, acquire broad heads, and extend laterally. Separation of the

pectoral girdle from the skull creates a neck allowing lateral movement of the head (relative to the

trunk). The endoskeletal scapulocoracoid is enlarged, buttressed, and reorients to face laterally.

Dermal bones of the pectoral girdle are reduced dorsally and laterally, but enlarged and expanded

ventrally. Not illustrated but of clear functional signiﬁcance, the pelvis enlarges and acquires direct

attachment, by means of one or more sacral ribs, to the vertebral column. Associated with this,

the hip socket (acetabulum) and surrounding buttresses are reoriented, as in the scapulocoracoid,

to face laterally.

Finally, scale coverage of the body and ﬁns is reduced dramatically in limbed tetrapods relative

to elpistostegalids (and other ﬁnned stem-taxa; Figure 4f). In early limbed tetrapods, ossiﬁed

scales are present only as gastralia, scales on the ventral surface of the trunk [Ichthyostega presents

a notable exception, with reported cycloid scales on the tail ( Jarvik 1952)].

THE ORIGIN OF TETRAPOD LIMBS: MORPHOLOGICAL NOVELTY

The ﬁn-to-limb transition concerns separate events at pectoral and pelvic levels, and there is

evidence that several changes occurred ﬁrst at pelvic level (Coates et al. 2002). The following

summary focuses on forelimbs because the data set is slightly more detailed. Key events concern ﬁn

ray loss, digit acquisition, and remodeling of the humerus. The resultant tripartite organization as

stylopod (humerus), zeugopod (radius and ulna), and autopod (wrist and digits) presumably reﬂects

the phylogenetic emergence of developmental autonomy within the outgrowing limb, in which

the zeugopod initially resembles a carry-over from the primitive (ﬁn) condition (Figure 4a–g).

Figure 4 shows Devonian and Carboniferous tetrapod pectoral ﬁn and limb endoskeletons.

Tetrapod ﬁn skeletons (Figure 4a–g) are clearly different from limb skeletons, and, as argued by

Rosen et al. (1981), they retain an essentially primitive, asymmetrically branched pattern (Friedman

et al. 2007). Within a phylogeny of tetrapod ﬁns and limbs, the longest internal branch (length

proportional to total character-state change) spans the ﬁn-to-limb divide (Coates et al. 2002).

Only the Late Devonian Catskill humerus (Shubin et al. 2004) slots into this gap, and the question

of whether it supported ﬁn rays or digits remains unanswered.

All ﬁns shown (Figure 4a–g) supported ossiﬁed and segmented ﬁn rays, and, in life, the en-

doskeleton was encased within a scale-covered muscular lobe (only shown in Figure 4f). Primi-

tively, the radius is consistently longer than the ulna. The humerus has been described as the ﬁrst

mesomere or segment of an axis drawn through the ulna and ulnare toward the outermost extrem-

ity of the ﬁn. Usually labeled the metapterygial axis (Coates 2003, Grandel 2003), this easily maps

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defg

Humerus

Radius

Ulna

Figure 4

Fin and limb skeletons. (a)Sauripterus, a rhizodont, after Davis et al. (2004a). (b)Barameda, a rhizodont, after

Long (1989) and Garvey et al. (2005). (c)Tiktaalik, an elpistostegalid, after Shubin et al. (2006).

(d)Eusthenopteron, a tristichopterid, after Andrews & Westoll (1970). (e)Gogonasus, an osteolepidid, after

Long et al. (2006). ( f)Sterropterygion, a megalichthyid (original). (g)Rhizodopsis, a megalichthyid, after

Friedman et al. (2007). (h)Acanthostega, a limb-bearing stem tetrapod, after Coates (1996). (i)Tulerpeton,a

limb-bearing stem tetrapod, after Lebedev & Coates (1995). ( j)Greererpeton, a limb-bearing stem tetrapod,

after Coates (1996). (k)Westlothiana, a stem amniote, after Smithson et al. (1994). Dermal ﬁn skeleton,

comprising ﬁn rays and scales, are shown in light gray for Sterropterygion (f); similarly elaborate dermal

skeletons are present, but not illustrated, in all taxa in the top two rows. These features are absent from the

digit-bearing taxa in the bottom row. All skeletons are shown with leading edge to right of Figure; all are in

dorsal aspect except for (a) and ( f) (ventral aspect).

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out to the third or fourth mesomere, but the pattern is often indistinct distally (Friedman et al.

2007). None of these skeletons is outstandingly limb-like. Although the pectoral ﬁn of Tiktaalik

(Figure 4c) is related most closely to digit-bearing limbs (Shubin et al. 2006), unambiguously

limb-like characteristics are restricted to humerus shape.

Digits can be regarded as a subgroup of radials, but they possess distinguishing characteristics,

including alignment as a series across the distal end of the appendage (functionally uniting distal

ends of the radius and ulna) and the absence of a distally branched pattern. Furthermore, digits

are known only in appendages where ﬁn rays and scales are absent. In primitive limb skeletons

(Figure 4h–k) the humerus is L-shaped with a large, posterior ﬂange, the entepicondyle. There

is a distinct elbow joint; distal to this the limb skeleton is generally ﬂexed (contrast Figure 4h–k

with 4a–i ). Several trends are apparent from the most primitive (Acanthostega, Figure 4h) to the

most advanced (Westlothiana, Figure 4k) examples shown. The humerus gains a shaft; the ulna

extends to equal radius length; the intermedium is moved into the wrist region (instead of ﬂanking

the radius); a complex wrist joint (including a noncylindrical intermedium) intercalates between

the radius, ulna, and digits; and digit numbers diminish to stabilize at ﬁve.

THE ORIGIN OF TETRAPOD LIMBS: DEVELOPMENTAL CHANGE

Most information about vertebrate limb development has been obtained from studies of chicks

and mice [reviewed recently by Tanaka & Tickle (2007)]. Fin data are largely from the teleost

zebraﬁsh (Grandel 2003), although further data are being obtained from paddleﬁsh (nonteleost

actinopterygians) (Davis et al. 2007, Metscher et al. 2005), lungﬁsh (sarcopterygians) ( Johanson

et al. 2007), and elasmobranch chondrichthyans (Dahn et al. 2007, Freitas et al. 2007). Importantly,

it appears that bony ﬁshes as a whole (from tetrapods to teleosts) share most of the same genes

and developmental regulatory systems, and that most of the same materials examined thus far are

deployed and used similarly in paired ﬁn buds and limb buds.

Digit primordia appear late in limb bud development, and some of the most widely discussed

work on this aspect of limb development concerns the similarly late and distal activity of particular

Hox genes and how this might affect digit patterning. Hox gene nested expression patterns in

outgrowing limb buds are dynamic and phased (Z´

ak´

any et al. 1997) and relate to proximodistal

patterning (Wellik & Capecchi 2003, Tarchini & Duboule 2006). A subset of Hox genes is expressed

at high levels in the digit-forming region (Kmita et al. 2002), and this expression phase was thought

to be absent in paired ﬁns. Functional studies provide important clues about the signiﬁcance of this

episode in digit development, as well as the evolutionary assembly of this regulatory architecture

(Kmita et al. 2002, Tarchini & Duboule 2006, Z ´

ak´

any et al. 1997). These data contributed to the

notion of the distal region of tetrapod limbs, including digits and the wrist/ankle (the autopod),

as an evolutionary novelty (Wagner & Chiu 2001). However, discovery of an autopodial-like Hox

gene expression pattern in the developing paired ﬁns of osteichthyans and chondrichthyans (Davis

et al. 2007, Freitas et al. 2007) suggests otherwise (consistent with patches of Hox gene expression

in lungﬁsh ﬁns: Johanson et al. 2007). It appears increasingly likely that aspects of autopodial

developmental patterning are general characteristics of paired ﬁn buds in all gnathostomes. Just

as digits can be characterized as a new and precise arrangement of ﬁn radials, their development

probably co-opted more general patterns of gene regulatory activity (Friedman et al. 2007, Grandel

2003).

Unlike digits, ﬁn rays are unambiguously unique to ﬁns. Fin rays are components of the dermal

skeleton (rather than endoskeleton), and the dermal skeleton is a derivative of the neural crest.

Trunk crest has evident skeletogenic potential, although in living tetrapods this capacity is only

expressed by the cranial neural crest (McGonnell & Graham 2002). Fin rays develop within the

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apical fold of an embryonic ﬁn bud (Grandel 2003, Witten & Huysseune 2007) and this fold

is an outgrowth of the apical ectodermal ridge, a major signaling center involved in limb bud

development. Loss of ﬁn rays during the evolutionary origin of limbs implies signiﬁcant change in

the developmental activity of the apical ectodermal ridge. Proximodistal patterning, outgrowth,

and anteroposterior patterning result from complex feedback-linked signal systems between the

apical ridge and other signaling centers of limb and ﬁn buds. Moreover, experimental and clinical

studies show that large-scale morphological abnormalities occur when such signals are disrupted

(Tanaka & Tickle 2007).

These differences between ﬁns and limbs have barely been considered from a comparative

and evolutionary standpoint (Freitas et al. 2007): the transition from apical ectodermal ridge to

apical fold, the arrest or persistence (in development) of an apical signaling center, the possible

presence and inﬂuence of skeletogenic neural crest mesenchyme. Any or all of these probably

interlinked factors, subject to natural variation, seem likely to have provided the material basis for

morphologically signiﬁcant and perhaps rapid evolutionary change.

THE ORIGIN OF TETRAPOD LIMBS: FUNCTIONAL CHANGE

As in discussions of developmental change, scenarios of functional change at the ﬁn-to-limb

transition have focused on the endoskeleton, whereas the role of scales and ﬁn rays has been

neglected. The suggestion that limbs evolved in a primitively aquatic taxon is based on conjunction

of paddle-like limbs, grooved gill bars, and skeletally supported tail ﬁn in Acanthostega (Coates

1996, Clack 2002). However, this now accompanies discussions of load-bearing ﬁns in Tiktaalik

(Shubin et al. 2006) and other stem tetrapods (Boisvert 2005). These speculations need not be

mutually exclusive, because vertebrate exploitation of marginal aquatic habitats probably happened

under different ecological circumstances for a variety of tetrapod groups, just as occurs today for

many kinds of teleost ﬁshes (Graham 1997).

As for speculation about the biomechanics of limb-like ﬁns, few substantial studies have been

completed. Histological analysis of the paired ﬁn skeletons of Eusthenopteron (Figure 3, top;

Figure 4d) indicates that this stem tetrapod, at least, was wholly aquatic (Laurin et al. 2007).

Among the descriptions of walking gaits in living ﬁshes (Pridmore 1995, Wilga & Lauder 2001, Lu-

cifora & Vassallo 2002a) an axial-driven walking trot has been proposed as primitive for tetrapods

(Pridmore 1995). Perhaps within stem tetrapods this aquatic walking trot was superseded by a

pelvic-driven bipedal gait, because air-ﬁlled lungs would have supported the anterior trunk re-

gion. Such a scenario is consistent with the phylogenetic sequence of limb evolution, in which

conventional limb characteristics occur ﬁrst in pelvic appendages (Coates et al. 2002). Fossil track-

way data might deliver further insights (Clack 2002), but assigning Devonian tracks to the earliest

limbed tetrapods is especially difﬁcult, given the paddle-like form and orientation of primitive

hind limbs.

HABITATS AND PALEOBIOGEOGRAPHY

Thus far, the late Givetian to early Frasnian elpistostegalids are conﬁned to the fringe of Euramer-

ica (Daeschler et al. 2006) (Figure 5). The Euramerican fringe also includes the Vis´

ean midland

valley of Scotland, source of the earliest crown-group tetrapods. Sandwiched between these last

two groups, the earliest limbed (and less-certainly limbed) genera have been collected from a wide

area, including the Frasnian-Famennian of Euramerica, North China, and easternmost Gondwana

(Blieck et al. 2007). The paleoenvironments of these Late Devonian tetrapods range from prox-

imal, near-shore marine localities to continental, freshwater lakes and rivers (Blieck et al. 2007,

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Sites yielding

elpistostegalian-

grade taxa

Sites yielding taxa

known or believed

to be limb bearing

713

14 24

15 18 19 20 21 22

Lower

Carboniferous

359–318 Ma

Middle–Upper

Devonian

387–359 Ma

115

Figure 5

Devonian and Carboniferous paleogeographic maps (adapted, with permission, from originals by Ron Blakey, Northern Arizona

University) marked with numbers corresponding to the following important tetrapod localities (black numerals indicate localities

yielding elpistostegalid-grade taxa, whereas red numerals denote sites yielding forms either known or believed to have been limb

bearing). Middle and Upper Devonian sites (taxon lists adapted from Clack 2007): 1, Gauja Formation, Latvia and Estonia (upper

Givetian; Livoniana,Panderichthys); 2. Miguasha, Quebec, Canada (lower Frasnian; Elpistostege); 3. Fram Formation, Nunavut, Canada

(lower Frasnian; Tiktaalik); 4. Scat Crag, Scotland (upper Frasnian, Elginerpeton); 5. Velna-Ala, Latvia (upper Frasnian; Obruchevichthys);

6. Jemalong, New South Wales, Australia (upper Frasnian-lower Famennian; Metaxygnathus); 7. Gornostayevka quarry, Russia (lower

Famennian; Jakubsonia); 8. Aina Dal and Britta Dal formations, East Greenland (upper Famennian; Acanthostega,Ichthyostega, new

genus); 9. Evieux Formation, Belgium (upper Famennian; Ichthyostega-like form); 10. Catskill Formation, Pennsylvania, USA (upper

Famennian; Catskill humerus, Densignathus,Hynerpeton, whatcheerid-like form); 11. Ketleri and Pav¯

ari, Latvia (upper Famennian;

Ventastega); 12. Ningxia, China (upper Famennian; Sinostega); 13. Andreyevka-2, Russia (uppermost Famennian; Tulerpeton). Lower

Carboniferous sites (taxon lists adapted from Clack 2002, Milner et al. 1986): 14. Horton Bluff, Nova Scotia, Canada (Tournaisian);

15. Ballagan Formation, Scotland (middle Tournaisian; Pederpes); 16. Delta, Iowa, USA (lower Vis ´

ean; Whatcheeria); 17. Duckabrook

Formation, Queensland, Australia (lower Vis´

ean; Ossinodus); 18. Wardie, Scotland (lower Vis´

ean; Lethiscus); 19. East Kirkton, Scotland

(middle Vis´

ean; see text for taxon list); 20. Cheese Bay, Scotland (middle Vis´

ean; Casineria); 21. Gilmerton Quarry, Scotland (middle

Vis ´

ean; Crassigyrinus,Loxomma, colosteid); 22. Dora, Scotland (upper Vis´

ean; Crassigyrinus,Doragnathus,Eoherpeton,Proterogyrinus,

adelogyrinid); 23. Greer, West Virginia, USA (upper Vis´

ean-lower Serpukhovian; Greererpeton,Proterogyrinus); 24. The well-known

Joggins locality (Upper Carboniferous, mid-Bashkirian).

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Lebedev 2004). Paleocontinental reconstruction (Averbuch et al. 2005) indicates that all 10 noted

localities for what might be the earliest limbed tetrapods lie within 30◦of the estimated equator,

consistent with macroevolutionary ideas about cradles of diversity (Goldberg et al. 2005). How-

ever, it remains unclear whether this distribution is the result of collection bias. Marginal deposits

of Late Devonian age have not been fully exploited in Africa, South America, or Antarctica.

THE END DEVONIAN EXTINCTION AND RECOVERY

The Late Devonian extinction, marked by an estimated loss of between 70% and 82% of marine

species (McGhee 2001), extended from the latest Frasnian and into the Famennian. This drawn-

out biotic crisis has been correlated with global cooling ( Joachimski & Buggisch 2002, Streel et al.

2000), atmospheric change (Berner et al. 2007, Scott & Glasspool 2006, Algeo et al. 2001), and the

radiation of terrestrial plants leading to aquatic eutrophication and anoxia on an intercontinental

scale (Algeo et al. 2001). Furthermore, the Late Devonian was a period of intense tectonic activity,

with incipient collisions of continental crustal blocks including Laurussia, Gondwana, Kazakhstan,

and Siberia (Averbuch et al. 2005). These tectonic events closed entire oceanic domains (Figure 5),

had a widespread inﬂuence on other marine environments, and probably contributed to global

cooling (Averbuch et al. 2005, Blieck et al. 2007).

Tetrapods (the total group) originated prior to this episode of massive change, and by the end of

it, most of the group seems to have perished. The greening (aquatic and terrestrial) of continents,

from the late Silurian through to the Middle Devonian, was a late phase in a vast sequence of con-

tinental invasions (Labandeira 2005). But those processes that provided the structural and trophic

complexity necessary for terrestrial vertebrate life might also have been those that devastated the

tetrapod clade (Algeo et al. 2001).

The ∼15 million year post-Devonian trough in the record of limbed tetrapods (Clack 2002,

Ruta et al. 2003) is also apparent in the fossil history of terrestrial arthropods (Ward et al. 2006).

Absence of both groups throughout most of the Tournaisian has been attributed (Ward et al.

2006) to an estimated trough in atmospheric oxygen levels (Berner et al. 2007), constraining

both groups to aquatic habitats. Physiological arguments have some bearing on this scenario,

but the sudden diversity of Vis´

ean limbed tetrapods implies that this gap might equally reﬂect

unevenness of the fossil record (Clack 2007). Tetrapod phylogeny clearly underwent multiple

branching events and encompassed considerable morphological diversiﬁcation during this interval,

the results of which include a¨

ıstopods, adelogyriniids, temnospondyls, and Westlothiana (and we

have correspondingly little idea about any hidden diversity of as yet unknown post-Devonian

elpistostegalids, “acanthostegids,” and ichthyostegids). If there is any signature in the tetrapod

record that might be more safely attributed to early Carboniferous atmospheric conditions, then

it is the reduced size of these crown tetrapods and their close relatives (Figure 2), compared with

the larger dimensions of earlier and more basally branching clades (Clack 2007).

CONCLUSIONS AND FUTURE DIRECTIONS

Early tetrapod distribution is clumpy at any scale, from detailed features of anatomy (note the

almost bimodal array paired ﬁn and limb skeletons; Figure 4) up to the patchy distribution of

body shapes and higher taxonomic categories. These patterns should be investigated; it seems

unlikely that they result wholly from extinctions editing chunks from evenly spread morphological

continuity (cf. Erwin 2007). The use of nontraditional node-based rather than character-based

group deﬁnitions is disputed (Blieck et al. 2007, Clack 2007), but it permits a better perspective

of early tetrapod evolution, and provides an explicit means of framing questions about group

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origins and change. The “vast structural gaps” (Milner et al. 1986) separating Ichthyostega from

osteolepiforms and Carboniferous tetrapods have effectively closed: The research program started

by Owen approximately 150 years ago is largely completed. Narratives of morphological change

from ﬁsh to tetrapod can be reﬁned, but there are other issues to address. The turnover in clade

composition across the Devono-Carboniferous boundary is dramatic, and we note that it yields

two groups that radiate signiﬁcantly within the post-Devonian Paleozoic: limbed tetrapods and

rhizodontids. If research explores only the limbed subset of the tetrapod total group, much of the

evolutionary signal will be missed (as if research on mammal evolution ignored noneutherians).

A detailed phylogenetic analysis of the whole of the tetrapod stem is needed. Similarly, Devonian

tetrapod-containing biotas need to be subjected to the level of study applied to Carboniferous

localities such as East Kirkton (Clarkson et al. 1994). Paleoecological understanding of the earliest

tetrapods would also be assisted by substantial biomechanical analyses of structures such as lobed

ﬁns, and vertebrae retaining a large notochordal component. Finally, developmental analyses

of differences between ﬁns and limbs, rather than searches for general, and perhaps primitive,

conditions, are more likely to improve our understanding of present and past morphological

diversity.

DISCLOSURE STATEMENT

The authors are not aware of any biases that might be perceived as affecting the objectivity of this

review.

ACKNOWLEDGMENTS

Much of what we currently understand about the early evolution of tetrapods is directly or in-

directly attributable to Alec Panchen (a signiﬁcant proportion of the work cited here might be

regarded as the output of his extended research group), and Stanley Wood (for discoveries of early

tetrapods and localities such as East Kirkton). Research is supported by the Faculty Research Fund,

Pritzker School of Medicine, University of Chicago (MIC); Environmental Protection Agency

STAR Fellowship (award number FP 916730; MF).

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Annual Review of

Ecology, Evolution,

and Systematics

Volume 39, 2008

Contents

Top Predators as Conservation Tools: Ecological Rationale,

Assumptions, and Efﬁcacy

Fabrizio Sergio, Tim Caro, Danielle Brown, Barbara Clucas, Jennifer Hunter,

James Ketchum, Katherine McHugh, and Fernando Hiraldo pppppppppppppppppppppppppppppppp1

Revisiting the Impact of Inversions in Evolution: From Population

Genetic Markers to Drivers of Adaptive Shifts and Speciation?

Ary A. Hoffmann and Loren H. Rieseberg ppppppppppppppppppppppppppppppppppppppppppppppppppp21

Radial Symmetry, the Anterior/Posterior Axis, and Echinoderm

Hox Genes

Rich Mooi and Bruno David pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp43

The Great American Schism: Divergence of Marine Organisms After

the Rise of the Central American Isthmus

H.A. Lessios pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp63

The Ecological Performance of Protected Areas

Kevin J. Gaston, Sarah F. Jackson, Lisette Cant´u-Salazar,

and Gabriela Cruz-Pi ˜n´on ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp93

Morphological Integration and Developmental Modularity

Christian Peter Klingenberg pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp115

Herbivory from Individuals to Ecosystems

Oswald J. Schmitz ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp133

Stoichiometry and Nutrition of Plant Growth in Natural Communities

G¨oran I. ˚

Agren pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp153

Plague Minnow or Mosquito Fish? A Review of the Biology

and Impacts of Introduced Gambusia Species

Graham H. Pyke pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp171

The Impact of Natural Selection on the Genome: Emerging Patterns

in Drosophila and Arabidopsis

Stephen I. Wright and Peter Andolfatto ppppppppppppppppppppppppppppppppppppppppppppppppppp193

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Sanctions, Cooperation, and the Stability of Plant-Rhizosphere

Mutualisms

E. Toby Kiers and R. Ford Denison ppppppppppppppppppppppppppppppppppppppppppppppppppppppppp215

Shade Tolerance, a Key Plant Feature of Complex Nature

and Consequences

Fernando Valladares and ¨

Ulo Niinemets ppppppppppppppppppppppppppppppppppppppppppppppppppp237

The Impacts of Fisheries on Marine Ecosystems and the Transition to

Ecosystem-Based Management

Larry B. Crowder, Elliott L. Hazen, Naomi Avissar, Rhema Bjorkland,

Catherine Latanich, and Matthew B. Ogburn ppppppppppppppppppppppppppppppppppppppppppppp259

The Performance of the Endangered Species Act

Mark W. Schwartz pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp279

Phylogenetic Approaches to the Study of Extinction

Andy Purvis pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp301

Adaptation to Marginal Habitats

Tadeusz J. Kawecki pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp321

Conspeciﬁc Brood Parasitism in Birds: A Life-History Perspective

Bruce E. Lyon and John McA. Eadie ppppppppppppppppppppppppppppppppppppppppppppppppppppppp343

Stratocladistics: Integrating Temporal Data and Character Data

in Phylogenetic Inference

Daniel C. Fisher ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp365

The Evolution of Animal Weapons

Douglas J. Emlen pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp387

Unpacking β: Within-Host Dynamics and the Evolutionary Ecology

of Pathogen Transmission

Michael F. Antolin ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp415

Evolutionary Ecology of Figs and Their Associates: Recent Progress

and Outstanding Puzzles

Edward Allen Herre, K. Charlotte Jand´er, and Carlos Alberto Machado pppppppppppppppp439

The Earliest Land Plants

Patricia G. Gensel ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp459

Spatial Dynamics of Foodwebs

Priyanga Amarasekare pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp479

Species Selection: Theory and Data

David Jablonski pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp501

vi Contents

Annu. Rev. Ecol. Evol. Syst. 2008.39:571-592. Downloaded from arjournals.annualreviews.org

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New Answers for Old Questions: The Evolutionary Quantitative

Genetics of Wild Animal Populations

Loeske E.B. Kruuk, Jon Slate, and Alastair J. Wilson pppppppppppppppppppppppppppppppppppp525

Wake Up and Smell the Roses: The Ecology and Evolution

of Floral Scent

Robert A. Raguso pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp549

Ever Since Owen: Changing Perspectives on the Early Evolution

of Tetrapods

Michael I. Coates, Marcello Ruta, and Matt Friedman ppppppppppppppppppppppppppppppppppp571

Pandora’s Box Contained Bait: The Global Problem of Introduced

Earthworms

Paul F. Hendrix, Mac A. Callaham, Jr., John M. Drake, Ching-Yu Huang,

Sam W. James, Bruce A. Snyder, and Weixin Zhang pppppppppppppppppppppppppppppppppppppp593

Trait-Based Community Ecology of Phytoplankton

Elena Litchman and Christopher A. Klausmeier pppppppppppppppppppppppppppppppppppppppppp615

What Limits Trees in C4Grasslands and Savannas?

William J. Bond ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp641

Indexes

Cumulative Index of Contributing Authors, Volumes 35–39 ppppppppppppppppppppppppppp661

Cumulative Index of Chapter Titles, Volumes 35–39 pppppppppppppppppppppppppppppppppppp665

Errata

An online log of corrections to Annual Review of Ecology, Evolution, and Systematics

articles may be found at http://ecolsys.annualreviews.org/errata.shtml

Contents vii

Annu. Rev. Ecol. Evol. Syst. 2008.39:571-592. Downloaded from arjournals.annualreviews.org

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Air Breathing and Suction Feeding Kinematics in the West African Lungfish, Protopterus Annectens

Article

Full-text available

Jul 2022

Research on the water-to-land transition tends to focus on the locomotor changes necessary for terrestriality. But the evolution from water breathing to air breathing was also a necessary precursor to the invasion of land. Air is approximately 1,000 times less dense, 50 times less viscous, and contains hundreds of times more oxygen than water. However, unlike the transition to terrestrial locomotion, breathing air does not require body weight support, so the evolution of air breathing may have necessitated smaller changes to morphology and function. We used X-ray Reconstruction of Moving Morphology to compare the cranial kinematics of aquatic buccal pumping, such as seen in suction feeding, with the aerial buccal pumping required for lung ventilation in the West African lungfish (Protopterus annectens). During buccal pumping behaviors, the cranial bones and associated soft tissues act as valves and pumps, and the sequence of their motions controls the pattern of fluid flow. Both behaviors are characterized by an anterior-to-posterior wave of expansion and an anterior-to-posterior wave of compression. We found that the pectoral girdle and cranial rib rotate consistently during air breathing and suction feeding, and that the muscle between them shortens during buccal expansion. Overall, we conclude that the major cranial bones maintain the same basic functions (i.e., acting as valves or pumps, or transmitting power) across aquatic and aerial buccal pumping. The cranial morphology that enables aquatic buccal pumping is well-suited to perform air-breathing and accommodates the physical differences between air and water.

Early onset of urea synthesis and ammonia detoxification pathways in three terrestrially developing frogs

Article

Full-text available

Aug 2023
J COMP PHYSIOL B

Frogs evolved terrestrial development multiple times, necessitating mechanisms to avoid ammonia toxicity at early stages. Urea synthesis from ammonia is a key adaptation that reduces water dependence after metamorphosis. We tested for early expression and plasticity of enzymatic mechanisms of ammonia detoxification in three terrestrial-breeding frogs: foam-nest-dwelling larvae of Leptodactylus fragilis (Lf) and arboreal embryos of Hyalinobatrachium fleischmanni (Hf) and Agalychnis callidryas (Ac). Activity of two ornithine-urea cycle (OUC) enzymes, arginase and CPSase, and levels of their products urea and CP in tissues were high in Lf regardless of nest hydration, but reduced in experimental low- vs. high-ammonia environments. High OUC activity in wet and dry nests, comparable to that under experimental high ammonia, suggests terrestrial Lf larvae maintain high capacity for urea excretion regardless of their immediate risk of ammonia toxicity. This may aid survival through unpredictably long waiting periods before rain enables their transition to water. Moderate levels of urea and CP were present in Hf and Ac tissues and enzymatic activities were lower than in Lf. In both species, embryos in drying clutches can hatch and enter the water early, behaviorally avoiding ammonia toxicity. Moreover, glutamine synthetase was active in early stages of all three species, condensing ammonia and glutamate to glutamine as another mechanism of detoxification. Enzyme activity appeared highest in Lf, although substrate and product levels were higher in Ac and Lf. Our results reveal that multiple biochemical mechanisms of ammonia detoxification occur in early life stages of anuran lineages that evolved terrestrial development.

The origin of blinking in both mudskippers and tetrapods is linked to life on land

Article

Full-text available

Apr 2023
P NATL ACAD SCI USA

Blinking, the transient occlusion of the eye by one or more membranes, serves several functions including wetting, protecting, and cleaning the eye. This behavior is seen in nearly all living tetrapods and absent in other extant sarcopterygian lineages suggesting that it might have arisen during the water-to-land transition. Unfortunately, our understanding of the origin of blinking has been limited by a lack of known anatomical correlates of the behavior in the fossil record and a paucity of comparative functional studies. To understand how and why blinking originates, we leverage mudskippers (Oxudercinae), a clade of amphibious fishes that have convergently evolved blinking. Using microcomputed tomography and histology, we analyzed two mudskipper species, Periophthalmus barbarus and Periophthalmodon septemradiatus, and compared them to the fully aquatic round goby, Neogobius melanostomus. Study of gross anatomy and epithelial microstructure shows that mudskippers have not evolved novel musculature or glands to blink. Behavioral analyses show the blinks of mudskippers are functionally convergent with those of tetrapods: P. barbarus blinks more often under high-evaporation conditions to wet the eye, a blink reflex protects the eye from physical insult, and a single blink can fully clean the cornea of particulates. Thus, eye retraction in concert with a passive occlusal membrane can achieve functions associated with life on land. Osteological correlates of eye retraction are present in the earliest limbed vertebrates, suggesting blinking capability. In both mudskippers and tetrapods, therefore, the origin of this multifunctional innovation is likely explained by selection for increasingly terrestrial lifestyles.

Evolution of the Vascular Pattern in Mammals: Using Synchrotron Imaging to Visualise Hidden 3D Structures

Thesis

Full-text available

Jun 2017

Jasper Ponstein

The morphology and histology of long bones are important tools for understanding tetrapod locomotion and growth. In mammals, the epiphyses of long bones ossify from a secondary centre of ossification. The consensus is that vascular canals are closely tied to the formation of these centres. However, the epiphyseal vascular organisation differs significantly between each major clade of mammals: Eutheria, Metatheria and Monotremata. Previous studies on the distribution of canals mainly examined 2D thinsections, which has led to inaccurate interpretations of their three-dimensionality. This study uses propagation phase-contrast X-ray microtomography to visualise the epiphyseal vascularisation of humeri from the eutherian Dasypus novemcinctus, the metatherian Didelphis marsupialis and the monotreme Tachyglossus aculeatus in 3D, to update on the known variability in extant mammals. Additionally, humeri from two stem-mammals, Galesaurus planiceps and Morganucodon sp., are included to infer the ancestral condition for Mammalia. Two types of canals are considered; piercing canals that pierce through the metaphysis, and cartilage canals that are connected to the perichondrium. Cartilage canals are reported in D. marsupialis, where these were previously thought to be absent. Traces of cartilage canals are also found in Morganucodon sp. Both fossil taxa exhibit piercing canals, as in monotremes and eutherians, although the canals are more numerous in the fossils. The distribution of cartilage canals therefore is wider than previously assumed. This new fossil data shows that both types of canals have evolved within the mammalian stem-group, thereby suggesting that the process involving both types of canals for ossifying epiphyses is relatively ancient.

A new elpistostegalian from the Late Devonian of the Canadian Arctic

Article

Full-text available

Aug 2022
NATURE

A fundamental gap in the study of the origin of limbed vertebrates lies in understanding the morphological and functional diversity of their closest relatives. Whereas analyses of the elpistostegalians Panderichthys rhombolepis , Tiktaalik roseae and Elpistostege watsoni have revealed a sequence of changes in locomotor, feeding and respiratory structures during the transition 1–9 , an isolated bone, a putative humerus, has controversially hinted at a wider range in form and function than now recognized 10–14 . Here we report the discovery of a new elpistostegalian from the Late Devonian period of the Canadian Arctic that shows surprising disparity in the group. The specimen includes partial upper and lower jaws, pharyngeal elements, a pectoral fin and scalation. This new genus is phylogenetically proximate to T. roseae and E. watsoni but evinces notable differences from both taxa and, indeed, other described tetrapodomorphs. Lacking processes, joint orientations and muscle scars indicative of appendage-based support on a hard substrate ¹³ , its pectoral fin shows specializations for swimming that are unlike those known from other sarcopterygians. This unexpected morphological and functional diversity represents a previously hidden ecological expansion, a secondary return to open water, near the origin of limbed vertebrates.

The Invasion of the Land in Deep Time: Integrating Paleozoic Records of Paleobiology, Ichnology, Sedimentology, and Geomorphology

Article

May 2022

Synopsis The invasion of the land was a complex, protracted process, punctuated by mass extinctions, that involved multiple routes from marine environments. We integrate paleobiology, ichnology, sedimentology, and geomorphology to reconstruct Paleozoic terrestrialization. Cambrian landscapes were dominated by laterally mobile rivers with unstable banks in the absence of significant vegetation. Temporary incursions by arthropods and worm-like organisms into coastal environments apparently did not result in establishment of continental communities. Contemporaneous lacustrine faunas may have been inhibited by limited nutrient delivery and high sediment loads. The Ordovician appearance of early land plants triggered a shift in the primary locus of the global clay mineral factory, increasing the amount of mudrock on the continents. The Silurian-Devonian rise of vascular land plants, including the first forests and extensive root systems, was instrumental in further retaining fine sediment on alluvial plains. These innovations led to increased architectural complexity of braided and meandering rivers. Landscape changes were synchronous with establishment of freshwater and terrestrial arthropod faunas in overbank areas, abandoned fluvial channels, lake margins, ephemeral lakes, and inland deserts. Silurian-Devonian lakes experienced improved nutrient availability, due to increased phosphate weathering and terrestrial humic matter. All these changes favoured frequent invasions to permament establishment of jawless and jawed fishes in freshwater habitats and the subsequent tetrapod colonization of the land. The Carboniferous saw rapid diversification of tetrapods, mostly linked to aquatic reproduction, and land plants, including gymnosperms. Deeper root systems promoted further riverbank stabilization, contributing to the rise of anabranching rivers and braided systems with vegetated islands. New lineages of aquatic insects developed and expanded novel feeding modes, including herbivory. Late Paleozoic soils commonly contain pervasive root and millipede traces. Lacustrine animal communities diversified, accompanied by increased food-web complexity and improved food delivery which may have favored permanent colonization of offshore and deep-water lake environments. These trends continued in the Permian, but progressive aridification favored formation of hypersaline lakes, which were stressful for colonization. The Capitanian and end-Permian extinctions affected lacustrine and fluvial biotas, particularly the invertebrate infauna, although burrowing may have allowed some tetrapods to survive associated global warming and increased aridification.

Using salamanders as model taxa to understand vertebrate feeding constraints during the late Devonian water-to-land transition

Article

Full-text available

Oct 2023

The vertebrate water-to-land transition and the rise of tetrapods brought about fundamental changes for the groups undergoing these evolutionary changes (i.e. stem and early tetrapods). These groups were forced to adapt to new conditions, including the distinct physical properties of water and air, requiring fundamental changes in anatomy. Nutrition (or feeding) was one of the prime physiological processes these vertebrates had to successfully adjust to change from aquatic to terrestrial life. The basal gnathostome feeding mode involves either jaw prehension or using water flows to aid in ingestion, transportation and food orientation. Meanwhile, processing was limited primarily to simple chewing bites. However, given their comparatively massive and relatively inflexible hyobranchial system (compared to the more muscular tongue of many tetrapods), it remains fraught with speculation how stem and early tetrapods managed to feed in both media. Here, we explore ontogenetic water-to-land transitions of salamanders as functional analogues to model potential changes in the feeding behaviour of stem and early tetrapods. Our data suggest two scenarios for terrestrial feeding in stem and early tetrapods as well as the presence of complex chewing behaviours, including excursions of the jaw in more than one dimension during early developmental stages. Our results demonstrate that terrestrial feeding may have been possible before flexible tongues evolved. This article is part of the theme issue ‘Food processing and nutritional assimilation in animals’.

Computed tomography and three-dimensional reconstruction of the skull of the stem tetrapod Crassigyrinus scoticus Watson, 1929

Article

May 2023

The early tetrapod Crassigyrinus scoticus was a large aquatic predator known from the lower- to mid-Carboniferous (upper Tournasian to upper Visean/lower Serpukovian, approximately 350–330 Ma) of Scotland and Canada. Crassigyrinus is enigmatic in terms of its phylogenetic position due to its unusual morphology, which features a mixture of primitive and derived characters. Previous reconstructions, based on five incomplete and deformed specimens, have suggested a dorsoventrally tall skull with a short and broad snout, large orbits and external nares, and an extended postorbital region. In this study, we scanned four specimens using computed tomography and segmented imaging data to separate bone from matrix and individual bones from each other. Based on these data, we present a revised description of the upper and lower jaws, including sutural morphology and abundant new anatomical information. Damage was repaired and the skull retrodeformed to create a hypothetical three-dimensional reconstruction of the skull of Crassigyrinus that is dorsoventrally flatter than earlier reconstructions, yet still morphologically unique amongst early tetrapods. Overall skull shape, the size and distribution of the teeth, sutural morphology, and the specialized anatomy of the jaw joint and mandibular symphysis all suggest that Crassigyrinus was a powerful aquatic predator capable of hunting and subduing large prey.

Decreased heat sensitivity of lungfish TRPV1 revealed by the heterologous expression system

Article

Mar 2023
BIOCHEM BIOPH RES CO

In this study, we focused on TRPV1 of African lungfish, Protopterus annectens. During drought at high temperature, African lungfish can survive by undergoing into aestivation in mud cocoons. Therefore, lungfish is considered to have some specialized heat-sensor, TRPV1, for heat tolerance. Further, lungfish which shares similarities with fishes and amphibians, is one of important species for investigating the fish-tetrapod transition. Since fish TRPV1 and tetrapod TRPV1 have some differences, character of lungfish TRPV1 attracts attention. Here, we first cloned TRPV1 paralogue from lungfish, Protopterus annectens (lfTRPV1) and determined the chemical and thermal sensitivities of lfTRPV1 by two-electrode voltage clamp method using frog oocytes. We detected activation of lfTRPV1 by acid and 2-APB, but capsaicin-induced activation was not observed. The sensitivity to acid of lfTRPV1 was similar to that of rat TRPV1 (rTRPV1), but the 2-APB sensitivity of lfTRPV1 was relatively weaker than rTRPV1. Heat stimulation up to 44 °C did not activate lfTRPV1 and the heat-activation was not detected even on acid condition of pH6. This dramatically decreased heat-sensitivity of TRPV1 may contribute the heat tolerance of African lungfish. Moreover, this might be the property of ancient tetrapod-type TRPV1 gene.

Vertebrate predation in the Late Devonian evidenced by bite traces and regurgitations: implications within an early tetrapod freshwater ecosystem

Article

Aug 2022

The terrestrialization process by vertebrates occurred during the Devonian period, with fully land-dwelling tetrapods recorded in the Carboniferous. Thus, the Late Devonian is an important period for deciphering the ecological pressures that applied during the water-to-land transition. Higher predation pressures in the underwater environment have been suggested as an influential biotic evolutionary factor in this key habitat shift. Direct evidence of ancient predation on Palaeozoic vertebrates is seen in the form of rare traces preserved on fossils, and these range from trauma observed on the skeleton (such as attack marks) to ingested food remains (bromalites). The late Famennian freshwater ecosystem of Strud (Belgium) consists of a rich assemblage of many coeval gnathostomes or jawed fishes (placoderms, ‘acanthodians’, actinopterygians, and various sarcopterygian groups including tetrapods). Here we analyse the record of direct evidence for predation in the Strud vertebrate fossil assemblage. We recognize 12 regurgitalites and 13 bite traces, including a rare case of a tooth embedded in its original prey body target. Fossils from regurgitalites were imaged using scanning electron microscopy and chemically analysed to test for their possible ingestion signature by comparison with other isolated skeletal remains from the same locality. From this evidence, tristichopterid tetrapodomorphs are inferred to be the highest consumers of the trophic network, targeting small placoderms, and porolepiforms, and probably congeners. We observe two possible prey patterns in regurgitalites, for sarcopterygians and actinopterygians, both of which are associated with acanthodians. In Strud, no trophic position can be deduced for tetrapods from direct fossil evidence of predation.

12. Effects of the Middle to Late Devonian Spread of Vascular Land Plants on Weathering Regimes, Marine Biotas, and Global Climate: Evolutionary and Environmental Perspectives

Chapter

Full-text available

Jan 2001

Mandibles of rhizodontids: anatomy, function and evolution within the tetrapod stem-group

Article

Full-text available

Jan 2003

Jonathan Jeffery

The Rhizodontida (Pisces: Sarcopterygii) is a clade of predatory fishes from the Upper Devonian (Aztecia; ?Givetian of Antarctica) through to the Upper Carboniferous (Strepsodus; Moscovian of northern Europe and North America). They form the most basal plesion within the tetrapod stem-lineage. The mandibles were dominated by large symphysial tusks on the dentary. Not much else is known of the mandibles in primitive rhizodontids. However, later forms show several derived characters: the mandible is very deep dorsoventrally and narrow linguolabially; the coronoid fangs bear only a single fang and no other dentition; the Meckelian element was unossified, leaving the adductor fossa unfloored by bone; the prearticular produced a large dorsal process lingual to the adductor fossa, presumably for muscle attachment. These and other characters are discussed in the context of the evolution of the tetrapod stem-group. The mandible appears to have been split into two functional units, one comprising the firmly sutured prearticular, coronoids and dentary, the other comprising the firmly sutured infradentaries. The connection between the two units was weak, suggesting a longitudinal intramandibular hinge. The possibility that this acted as a 'torsion grip' during feeding is discussed.

Lithostratigraphic revisions of the upper Carboniferous to lower Permian strata in the Cumberland Basin, Nova Scotia and the regional implications for the Maritimes Basin in Atlantic Canada

Article

Full-text available

Jan 1991

The Cumberland Basin is a key area in the regional nomenclature because it contains the type sections of the Cumberland and Pictou groups, and well exposed sections of strata traditionally assigned to the Riversdale group (abandoned) and Canso group (abandoned and replaced by the Mabou Group). The constitutent formations of the Cumberland and Pictou groups examined by this study include in ascending order: Cumberland Group, 1. Claremont and 2. Boss Point, (both formerly assigned to the Riversdale group, now abandoned); 3. Polly Brook (new); 4. Joggins (redefined); 5. Springhill Mines (new); 6. Ragged Reef (new); 7. Malagash (new); and Pictou Group, 8. Balfron (new); 9. Tatamogouche (new); and 10. Cape John (redefined. The revised Pictou Group; includes all of the redbed dominated, non coal-bearing strata above the Cumberland Group. -from Authors

The Devonian tetrapod Ichthyostega

Chapter

Apr 1996

Erik Jarvik

2. A Comparison of Controversial Hypotheses on the Origin of Tetrapods

Chapter

Dec 1991

Hans-Peter Schultze

Description and systematics of panderichthyid fishes with comments on their relationship to tetrapods

Article

Jan 1991

Determinants of diversity in higher taxonomic categories

Article

Sep 1980

James W Valentine

It is often assumed that, if a few species are introduced into a relatively empty environment, the subsequent diversification will take the form of a logistic growth curve, rising to an equilibrium level of species richness. The diversifications of taxa in higher categories commonly resemble logistic curves, although there are no well-defined theoretical bases for such a resemblance. A model of diversification of taxa in higher categories is based on the notion that many taxa originate rapidly. Relatively small changes leading to new species occur at a high frequency, while larger changes leading to progressively higher taxa occur with progressive rarity. During diversification in an empty environment, few large changes will occur before the environment is filled. The rate of filling, relative to the rate of production of higher taxa, determines the richness of taxa in higher categories and gives the diversification curves a logistic appearance although the maximum level achieved is not an equilibrium. Subsequently, opportunities for diversification will generally lead only to the appearance of taxa in progressively lower categories.

The postcranial skeleton of Eustenopteron foordi Whiteaves

Article