Fossil Record 12 (1) 2009, 83–90 / DOI 10.1002/mmng.200800012

The largest specimen of and the life history pathway of neoteny in the temnospondyl family

Nadia B. Frbisch*,1 and Rainer R. Schoch2

1 Redpath Museum, McGill University, Montreal, Canada; Current address: Department of Biology, University of Toronto Mississauga, 3359 Mississauga Road, Mississauga, Ontario L5L 1C6, Canada; E-mail: [email protected] 2 Staatliches Museum fr Naturkunde Stuttgart, Rosenstein1, 70191 Stuttgart; Germany

Abstract

Received 9 June 2008 Two distinct developmental trajectories, and neoteny (the retention of Accepted 19 September 2008 larval somatic features in adult ), have been reported for the small gill-bearing Published 20 February 2009 branchiosaurids of the Late and Early of central Europe. Based on a very large specimen of the species Apateon caducus (Ammon, 1889), anatomical features characteristic for the neotenic of branchiosaurids are described. Large neotenes lack changes that occur during a short phase of transformation into terrestrial adults (metamorphosis), such as ossification of the braincase and palatoqua- drate and intercentra, further ossification of the girdles and formation of muscle attach- ment scars and processes on the limb bones. They also lack a distinct sculpturing of the dermal skull roofing elements with deep polygonal ridges and grooves. Instead, larval somatic features are retained including ossified branchial denticles indicative of Key Words open gill slits and accentuated larval-type sculpturing of the dermal skull roof. Large size, high degree of ossification as compared to the larvae, and the presence of unci- paedomorphosis nate processes on the ribs clearly demonstrate an adult ontogenetic stage. Neotenes metamorphosis remained in the aquatic environment throughout their life and were most likely not development capable of effective terrestrial locomotion. The frequency distribution of the two phe- notypes in modern populations and the environmental cues that influence Carboniferous the development of them provide a comparative framework for the discussion of the Permian evolution of the two life history pathways in branchiosaurids.

Introduction 1974; Milner 1982; Boy 1986, 1987; Schoch 1992, 1995; Boy & Sues 2000; Schoch 2002a; Schoch & Car- The small, gill-bearing Branchiosauridae represent the roll 2003; Schoch 2004; Frbisch et al. 2007), and phy- best-known within the diverse dissorophoid am- logeny (Schoch & Milner 2008) of branchiosaurids phibians of the Late Carboniferous and Early Permian. have been analyzed. They are particularly abundant in the lake depos- Despite the numbers of available specimens and its of central Europe and their fossil record is excep- knowledge of many aspects of branchiosaurid biology, tional due to the Lagersttten conditions of these local- it remained unresolved until recently whether branchio- ities and with assemblages of hundreds of specimens saurids represent larvae of animals that eventually me- representing various ontogenetic stages. Moreover, fea- tamorphosed into terrestrial adults or if they were neo- tures of their soft anatomy, such as the external gills tenic forms. The term neoteny (or ‘paedomorphosis’) is and ‘skin shadows’ are preserved in numerous speci- here used with reference to the retention of larval so- mens. Based on this excellent fossil record many as- matic features in sexually mature adults. pects of the ecology (Boy 1998; Boy & Sues 2000; The vast majority of branchiosaurid specimens repre- Werneburg 2002; Boy 2003), paleogeography (Werne- sent larval or perennibranchiate forms, and they have burg & Schneider 2006), (Boy 1971, 1972, been interpreted as neotenic. However, it has also been

* Corresponding author

# 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 84 Fro¨ bisch, N. B. & Schoch, R. R.: Neoteny in Branchiosauridae suggested that the absence of metamorphosed adults , based on observations on the ecology of that would have visited the lakes only seasonally for investigated salamander taxa (Sprules 1974; Whiteman mating, could be a result of the incomplete fossil re- 1994). cord, because very few specimens are known from the In modern salamanders, neoteny varies from obliga- shoreline or near shore terrestrial environment (Boy & torily neotenic forms, e.g. the Mexican Ambys- Sues 2000). Recently, specimens of the species Apateon toma mexicanum (Shaw & Nodder, 1789), where no gracilis (Credner, 1881), a small taxon that grew to ca. members of the species metamorphose under natural 22 mm in skull length and is exclusively known from conditions, to facultatively neotenic forms, e.g. the tiger the Niederhslich locality near Dresden, were identified salamander Ambystoma tigrinum (Green, 1825) or the that clearly represent metamorphosed adults (Boy 1987; red-spotted newt Notophthalmus viridescens (Rafi- Werneburg 1991). Based on a detailed analysis of the nesque, 1820). Obligatory neoteny arises when the fre- ontogenetic sequence of this taxon, we were able to de- quency of this morphotype increases under long-term monstrate that the complete developmental trajectories stable environmental conditions and eventually becomes observable in modern salamanders, i.e. neoteny and fixed (Whiteman 1994). While present in many sala- metamorphosis, were established in branchiosaurids mander taxa (Duellman & Trueb 1986), facultative neo- (Schoch & Frbisch 2006). Three distinct phases in the teny has been particularly well studied for various spe- development of Apateon gracilis were recognized: cies and populations of Ambystoma. Neoteny is (1) An early larval phase of steadily increasing bone considered to be triggered by a multitude of factors, count, (2) a phase of stagnation where no additional de- such as food availability, population density, size com- velopmental events took pace, but rather an overall in- position of a larval population, presence of predators, crease in size occured, and (3) a short phase in which presence of parasites or pathogens, and the specific ter- new events occurred in rapid succession which are as- restrial and aquatic conditions, whereas either a single sociated with a switch to a terrestrial habitat (metamor- factor or a combination of factors can act on different phosis). The findings showed that the tempo and mode populations (Snyder 1956; Anderson 1971; Wilbur & of metamorphosis is comparable to modern Collins 1973; Sprules 1974; Patterson 1978; Semlitsch and represents the first evidence for a condensed meta- & Gibbons 1985; Harris 1987, 1989; Harris et al. 1990; morphosis outside the . Semlitsch et al. 1990; Whiteman 1994; Shaffer & Voss Schoch & Frbisch (2006) discussed general aspects 1996). In particular harsh terrestrial conditions, such as of the neotenic trajectory in branchiosaurids. Here we severe temperature fluctuations, lack of cover, and low discuss the biological background and the available humidity, as well as the availability of permanent morphological evidence for neoteny in branchiosaurids bodies of water are considered to play a major role in in more detail, based on a previously undescribed, well- the occurrence of neotenic morphotypes (Snyder 1956; preserved specimen of a large Apateon caducus with a Sprules 1974; Whiteman 1994). These are often en- skull length of 38 mm from the Niederkirchen locality countered in high altitudes and Ambystoma populations in the Saar-Nahe region of western Germany (Figs 1, 2, in mountainous regions were found to develop neotenes 3B, C). Apateon caducus was previously known from most frequently (Snyder 1956; Sprules 1974; Whiteman specimens reaching a skull length of 24 mm (Fig. 3A) 1994). Nonetheless, even in completely neotenic popu- and like the smaller Apateon pedestris Meyer, 1844, lations evidence suggests that metamorphosis can be in- was widespread in the lakes of the Palatinate and Au- duced when aquatic conditions become very unfavor- tun. able as reflected in evaporation rate, salinity, oxygen content, and temperature (Sprules 1974). In other popu- lations, neotenic and metamorphosing individuals co- exist in the same ponds and their relative frequency de- Neoteny in modern salamanders pends on the local environmental parameters (Sprules Observations on the life history trajectories in branchio- 1974; Whiteman 1994; Denoel et al. 2002). saurids are best compared to modern salamanders, Whiteman (1994) formulated three hypotheses to ex- which are considered the most plesiomorphic of all ex- plain the occurrence and frequency distribution of neo- tant amphibians in terms of their morphology and life tenes in modern salamander populations: history (Duellman & Trueb 1986). They lack the highly (1) The neotenic advantage hypothesis explains the specialized tadpole of anurans and the highly presence of neotenic morphotypes in favorable aquatic modified life cycles of caecilians. habitats. Therein, neotenes have an advantage over me- Neotenic and metamorphic morphs of a single sala- tamorphosing morphs if the terrestrial conditions are mander species are a classic example for phenotypic harsh. The capacity for metamorphosis may still be plasticity, the ability of an individual organism to alter maintained in these populations if the aquatic condi- its phenotype in response to changes in environmental tions are occasionally unfavorable, e.g. in particularly conditions. It has frequently been suggested that pheno- dry years where most or all water of the pond/lake eva- typic plasticity is evolutionarily adaptive in many taxa porates. (West-Eberhard 2003) and more specifically with refer- (2) The ‘best of a bad lot’ hypothesis is the opposite ence to neotenic and metamorphosing morphotypes in of the neotenic advantage hypothesis. Therein larvae

museum-fossilrecord.wiley-vch.de # 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim Fossil Record 12 (1) 2009, 83–90 85 within a population that manage to reach a minimal hand and the Melanerpeton-clade on the other hand. body size for metamorphosis metamorphose into terres- The developmental pathway of metamorphosis is thus trial adults, while the smaller larvae become neotenes far exclusively known from the Apateon-clade and and thereby can reproduce at a smaller body size, mak- more specifically the species Apateon gracilis. In con- ing the ‘best of a bad lot’. trast, members of the Melanerpeton clade seem to be (3) Finally, the dimorphic neotene hypothesis repre- universally neotenic and several large specimens, likely sents a combination of the two hypotheses outlined representing adult neotenes are known for Melanerpe- above. It is possible that both conditions meet and pro- ton humbergense (Boy, 1978) and Melanerpeton eisfeldi duce two types of neotenes in the same population. The Werneburg, 1988 (A. Milner, pers. comm. 2008). largest and the smallest larvae become neotenic, while In addition to the adult Apateon gracilis specimen medium-sized larvae metamorphose. Therefore, similar that passed through a series of developmental events fi- life history mechanisms are favored for different reasons. nally transforming into clearly terrestrial adult animals This shows that neoteny in salamanders is a result of (Schoch & Frbisch 2006), large specimens of Apateon a complex interplay of environmental conditions result- pedestris and Apateon caducus have been recognized ing in different frequencies of the two life history stra- that lack these feature altogether. Nonetheless, they tegies. Changes in the population structure have also clearly differ from larval specimens and are identified been observed over time. Tihen (1942) investigated a as adult neotenes. The anatomical features associated fossil colony of Ambystoma tigrinum in a late Pleisto- with neoteny in branchiosaurids are discussed in detail cene sink in Kansas. The Pleistocene population con- on the basis of a very large, previously undescribed sisted predominantly of neotenic animals, coinciding specimen of Apateon caducus. with harsh terrestrial conditions that have been recon- Institutional abbreviations: BSP, Bayerische Staatsamm- structed for this locality in the Pleistocene. In contrast, lung fr Palontologie, Mnchen (Germany); GPIM, Ins- the terrestrial conditions are much more favorable for titut fr Geowissenschaften, Palontologie, Universitt salamanders today and Ambystoma tigrinum populations Mainz (Germany). in this area nowadays consist predominantly of meta- morphosing individuals. Given the complexity of fac- tors influencing the frequency of the two , it Description is not surprising that neotenic morphotypes were found to have evolved independently multiple times in sala- The specimen was collected at the Niederkirchen local- manders (Shaffer 1984). ity in the Pfalz region of southwestern Germany (Gzhe- lian). It is preserved on a slab and counter-slab (GPIM- N-9u2 and GPIM-N-9u2a) (Figs 1A, B, 2A, B, 3) and Evidence for neotenic morphotypes represents a very large individual with a skull length of in branchiosaurids 38 mm. The specimen consists of a well-preserved par- Schoch & Milner (2008) recognized two distinct tial skeleton comprising the skull in dorsal and ventral within Branchiosauridae, the Apateon-clade on the one views, as well as the anterior portion of the trunk and

Figure 1. Apateon caducus (Ammon, 1889), specimen GPIM-N-9u. A. Photograph of specimen; B. Drawing of specimen. Abbre- viations: bd – branchial denticles; cl – clavicle; d – dentary; h – humerus; ic – interclavicle; j – jugal; mc – metacarpals; mx – maxilla; n – nasal; na – neural arch; pal – palatine; pmx – premaxilla; pf – prefrontal; ph – phalanges; pof – postfrontal; pt – pterygoid; qj – quadratojugal; r – rib; ra – radius; s? – stapes?; sc – scapula; sq – squamosal; ul – ulna.

# 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim museum-fossilrecord.wiley-vch.de 86 Fro¨ bisch, N. B. & Schoch, R. R.: Neoteny in Branchiosauridae

Figure 2. Apateon caducus (Ammon, 1889), specimen GPIM-N-9u a (counterslab). A. Photograph of specimen; B. Drawing of shoulder girdle and forelimbs. For an explanation of abbreviations see Figure 1. the forelimbs. A ‘skin shadow’ is visible in the poster- Rows of branchial denticles are preserved on the ior region of the trunk, where faint impressions of the right lateral side of the specimen, located between the small scales that covered the body, are visible (Figs 1B, skull and the shoulder girdle (Figs 1, 2). Ossified bran- 2A). chial denticles were positioned along the endochondral GPIM-N-9u2 can be assigned to the species Apateon gill rakers with the latter providing a means to close caducus on the basis of its wide skull roof (IOW/ the gill slits during suction feeding, thereby producing Sl ¼ 0.32), the slender parietals, which are only slightly a greater negative pressure in the oral cavity. Branchial wider than the frontals, and the very wide, posterome- denticles on the gill rakers may have served as a filter- dially extended postfrontals (Boy 1987; Schoch 1992) ing device in larvae (Schoch 2001, 2002b; Schoch & (Figs 1A, B, 3). Although the prefrontal is not pre- Milner 2008). While soft tissue preservation of the ex- served in place, pre- and postfrontal probably ap- ternal gills does not occur in this specimen, the pre- proached each other closely, because the anterior pro- sence of ossified branchial denticles clearly indicates cess of the postfrontal reaches far anteriorly alongside that the had open gill clefts, which represent the two-thirds of the length of the frontal and the prefrontal most clear-cut anatomical evidence of an aquatic life- also shows a long posterior process (Figs 1A, B, 3). style in Paleozoic amphibians (Boy 1974; Schoch 2001, Pre- and postfrontal are clearly separated in larval 2002b). A. caducus specimens, but approach each other in older Changes in the ornamentation of the dermal skull individuals. Moreover, the robust palatine branch of the roofing elements have frequently been suggested to be pterygoid is strongly arcuate, a feature that is also typi- associated with metamorphosis in Paleozoic amphibians cally found in A. caducus (Boy 1987). (Bystrow 1935; Boy 1974; Schoch 2001; Schoch & The well-preserved posterior portion of the skull in Frbisch 2006) and indeed metamorphosed specimens specimen GPIM-N-9u shows that it lacks any ossifica- of Apateon gracilis display a pattern of pronounced tions of the endocranium and the jaw articulation was polygonal ridges and grooves otherwise never found in at the level or only slightly posterior to the posterior branchiosaurids. In contrast, specimen GPIM-N-9u end of the skull roof. shows a pattern of dermal ornamentation that consists

museum-fossilrecord.wiley-vch.de # 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim Fossil Record 12 (1) 2009, 83–90 87

which is also commonly seen in neotenic salamanders. However, it remains unknown whether ossified carpal and tarsal elements are present in metamorphosed A. gracilis, because this region is not preserved in the available specimens. The high degree of ossification in the limb skeleton, with well-developed muscle attach- ment areas and an ossified olecranon process in meta- morphosed A. gracilis indicate that metamorphs were primarily land-dwelling animals capable of an effective terrestrial locomotion. In a closely related group of small dissorophoid amphibians, the terrestrial Amphiba- midae, carpals and tarsals are frequently ossified (e.g. Daly 1994; Schoch & Rubidge 2005; Anderson et al. 2008) and it seems likely that the mesopodial region of metamorphosed branchiosaurids ossified as well. In comparison, the low degree of ossification and the lack of distinct processes and pronounced muscle attachment areas in the limb elements of specimen GPIM-N-9u contrasts strongly with the condition found in the meta- morphs of A. gracilis. The appendicular skeleton, parti- cularly the shoulder girdle, was overall weakly ossified and was most likely not suitable for effective support of a large branchiosaurid on land. Instead, adult A. ca- ducus presumably spent its life in an aquatic habitat, where most of its body weight was supported through Figure 3. Apateon caducus (Ammon, 1889). A. Previously lar- the buoyancy of the water. gest known complete skull from the Erdesbach locality; Interestingly, specimen GPIM-N-9u shows small un- B, C. Reconstruction of the large neotenic specimen from the cinate processes on some of the ribs lateral and slightly Niederkirchen locality. Abbreviations: f – frontal; j – jugal; l – lacrimal; m – maxilla; n – nasal; p – parietal; pf – prefrontal; distal to the widened rib head (Figs 1A, B, 2A). Unci- pm – premaxilla; po – postorbital; pof – postfrontal; pp – nate processes have not been reported in either mor- postparietal; qj – quadratojugal; sq – squamosal; st – supra- photype of branchiosaurids before. Large uncinate pro- temporal; t – tabular. cesses are known from other groups, e.g. the aquatic capitosaur (Schoch 1999), Ar- of pits in the central parts of individual skull roofing chegosaurus (Witzmann & Schoch 2006), Sclerocepha- bones and shallow grooves radiating out from this area, lus (Boy 1988), and Sclerothorax (Schoch et al. 2007). which represents and accentuated form of the larval Although their functional importance is unclear, they dermal ornamentation (Figs 1A, B, 3). usually formed in only adult specimens. Branchiosaur- The paired neural arches are the only ossified ele- ids had a rather short trunk and most probably did not ments in the vertebral column with central elements rely on lateral undulation of the body for locomotion, presumably remaining unossified. Ossified intercentra whereby uncinate processes would have hindered the are found only in metamorphosed specimens of the lateral movement. The tail, which bore a large fin as branchiosaurid Apateon gracilis. seen in many well-preserved specimens with soft tissue The elements of the shoulder girdle are overall small preservation (e.g. Werneburg 2002), served as the main with a small triangular interclavicle and slender clavi- tool for rapid propulsion in the aquatic environment, cles and cleithra. The small, ossified, and crescent- while the limbs might have been used for slow locomo- shaped scapular portion of the scapulacoracoid differs tion on the ground and for clinging to aquatic vegeta- strongly from the large, bony scapulocoracoid plates tion. The uncinate processes in specimen GPIM-N-9u present in metamorphosed Apateon gracilis. The radius possibly offered additional attachment areas for trunk and ulna of specimen GPIM-N-9u are well ossified and musculature in large, adult neotenes. have widened condylar ends and slender shafts, but lack distinct processes and muscle attachment scars (Figs 1, 2). All four metacarpals and digits of the right Discussion and conclusions manus, as well as three metacarpals and three phalan- geal elements of the left manus are preserved on slab With a skull length of 38 mm, GPIM-N-9u represents GPIM-N 9u2a (Figs 2A, B). Metacarpals and phalanges the largest known specimen within the extensive col- are well ossified and the terminal phalanges have an lections of Apateon. The combination of features, i.e. arcuate, pyramidal form, typical for late ontogenetic the large size, partially interdigitating and tight sutures stages of A. caducus and A. pedestris (Schoch 1992; of the skull roof, the high degree of ossification and Frbisch et al. 2007). The carpals remained unossified, differentiation of the postcranium as compared to

# 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim museum-fossilrecord.wiley-vch.de 88 Fro¨ bisch, N. B. & Schoch, R. R.: Neoteny in Branchiosauridae smaller larval specimens, and the presence of uncinate taneously with acanthodians and other branchiosaurid processes, indicates that this specimen represents an taxa (J. Boy, pers. comm. 2008). adult. However, it lacks ossifications of the exoccipi- This shows that branchiosaurids inhabiting the differ- tals and quadrates, intercentra, and the coracoid por- ent Paleozoic lakes were exposed to quite divergent en- tion of the scapulocoracoid as seen in metamorphosed vironmental conditions within the aquatic environment, specimens of Apateon gracilis. Moreover, larval so- comparable to the factors that are known to influence matic features are retained, such as the ossified bran- the frequency of neotenes in modern salamander popu- chial denticles indicative of the presence of open gill lations. Similar factors may also have influenced the de- slits and the accentuated larval-type sculpturing of the velopment and frequency of neotenic and metamorphic dermal skull roofing elements that demonstrate that morphotypes of different branchiosaurid populations, this animal was an adult neotene and lived in an but despite their excellent fossil record it remains im- aquatic habitat. possible to decipher specific environmental parameters The anatomical evidence at hand clearly indicates that may have acted on the particular branchiosaurid po- that both life history strategies, metamorphosis and pulations. Boy (2003) found evidence for the amphibian neoteny, were established in Paleozoic branchiosaurids. populations in the Odernheim and Niederkirchen lakes However, the specimens identified as adult neotenes to have been under stress, and that the genus Apateon and metamorphs, belong to different species of Apa- was apparently the most successful vertebrate to cope teon, i.e. A. caducus and A. gracilis, respectively. There- with unfavorable conditions. The neotenic pathway per- fore, there is at this time no direct evidence that bran- mitted Apateon to respond to external parameters by chiosaurids utilized facultative neoteny within a single (1) extending the early larval phase and stay a filter-fee- species (or even population) to accommodate to chan- der (A. pedestris) or (2) truncate the early phase, accel- ging environmental conditions, as observed in many erate growth, consolidate the connection between the modern salamander taxa. Nonetheless, in analogy with jaw and the cheek and form a larger predatory morpho- modern urodeles it is probable that branchiosaurids at type (A. caducus) (Schoch & Milner 2008). some point in their evolutionary history had a reaction While the lakes were located in the paleoequatorial norm with the full set of phenotypic responses to dif- region, monsoon-like weather patterns have been recon- ferent environmental cues (metamorphosis to neoteny) structed for this area in the Permo-Carboniferous (Pat- and likely were facultatively neotenic. Later, the fre- zowsky et al. 1991), resulting in significant variation in quency of one of the phenotypes may have increased in precipitation throughout the year (Clausing & Boy different taxa/populations under stable environmental 2000). In combination with the high altitude, this would conditions and this phenotype afterward became fixed. at least seasonally produce harsh conditions in the ter- Branchiosaurids are found in central European fossil restrial environment. The large size of the lakes sug- lakes, which during the Late Carboniferous and Early gests that they provided a permanent body of water Permian were located in the Variscian Mountains at an over long periods of time providing a sheltered, stable altitude of up to 2000 meters (Becq-Giraudon et al. environment for branchiosaurids and thereby promoting 1996; Boy & Schindler 2000). Most of the lakes that the development of neotenic morphotypes. Selection yielded branchiosaurids were very large and deep lakes should only favor plasticity (i.e. facultative neoteny) if with up to tens of kilometers in diameter. Boy (1998, environmental conditions are sufficiently spatially or 2003) and Boy & Sues (2000) reconstructed the paleo- temporally variable (Whiteman 1994). If the lakes pro- ecological successions of some of the branchiosaurid vided a constant favorable environment for branchio- bearing lakes of the Saar-Nahe Basin of western Ger- saurids as opposed to the terrestrial habitat, it is possi- many. This showed that small branchiosaurids, in parti- ble that the frequency of neotenes increased rapidly, cular A. pedestris, were founder taxa, initially coloniz- resulting in the dominance of this phenotype in the ing the lakes and later disappeared when or more branchiosaurid fossil record. specialized amphibian taxa appeared. However, some Certain terrestrial adaptations in the branchiosaurid lakes with an impoverished pelagic community (e.g. the , such the short trunk and long limbs suggest Odernheim and Ruthweiler lakes) do not show this suc- that branchiosaurids represent an initially terrestrial cession and A. pedestris co-occurs with larger carnivor- clade (Boy 1972; Boy & Sues 2000). The occurrence ous taxa such as A. caducus and Melanerpeton humber- of metamorphosed morphs in the phylogenetically gense. In the Niederkirchen lake, small branchiosaurids highly nested taxon Apateon gracilis would therefore such as A. pedestris were found to initially co-occur suggest a reversal to the metamorphosis trajectory in with fish. Later, only the acanthodian Acanthodes re- branchiosaurids (Schoch & Milner 2008). However, mains as fish representative and in addition the larger there may be manifold ecological or seasonal/deposi- branchiosaurids A. caducus and M. humbergense, and tional reasons for a selection of fossil preservation subsequently also the basal dissorophoid Micromelerpe- against terrestrial adults (Boy & Sues 2000). Therefore, ton credneri Bulman & Whittard, 1926 are present. the sparse fossil record of metamorphosed branchio- Specimen GPIM-N-9u derives from the latest phase saurids and the apparently overwhelming number of preserved in the succession of sediments (layer 9) of neotenes may at least in part be a relic of the fossil the Niederkirchen locality and inhabited the lake simul- record, providing only a biased and time averaged view

museum-fossilrecord.wiley-vch.de # 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim Fossil Record 12 (1) 2009, 83–90 89 of the evolution of branchiosaurid life history trajec- Karbon-Perm). 1. . – Palontologische Zeit- tories. schrift 62: 107–132. Nonetheless, an understanding of the patterns of life Boy, J. A. 1998. Mglichkeiten und Grenzen einer kosystem-Rekon- struktion am Beispiel des lakustrinen Palo-kosystems. 1. Theo- history trajectories in branchiosaurids provides impor- retische und methodische Grundlagen. – Palontologische Zeit- tant insights into the biology and evolution of this schrift 72 (1/2): 207–240. clade. Novel traits expressed as an alternative pheno- Boy, J. A. 2003. Palokologische Rekonstruktion von Wirbeltieren: type can undergo extensive evolution in a population Mglichkeiten und Grenzen. – Palontologische Zeitschrift 77 (1): and represent an important phase in the evolution of 123–152. major adaptive novelties characterizing species and Boy, J. A. & Schindler, T. 2000. kostratigraphische Bioevents im higher taxa (West-Eberhard 2003; Wiens et al. 2005). Grenzbereich Stephanium/Autunium (hchstes Karbon) des Saar- The plasticity in life history pathways of branchiosaur- Nahe-Beckens (SW-Deutschand) und benachbarter Gebiete. – Neues Jahrbuch fr Geologie und Palontologie Abhandlun- ids may have played an important role for the evolu- gen 216 (1): 89–152. tionary success and diversification of this Paleozoic Boy, J. A., & Sues, H.-D. 2000. Branchiosaurs: Larvae, metamorphosis amphibian clade. and in temnospondyls and seymouriamorphs. In Heat- wole, H. & Carroll, R. L. (eds). Amphibian Biology, Volume 4, Pa- laeontology. Surrey Beatty & Sons, Chipping Norton: pp. 1151–1197. Acknowledgements Bulman O. M. B. & Whittard, W. F. 1926. On and al- lied genera (Amphibia). – Proceedings of the Zoological Society We would like to thank Axel Friebe and Michael Wuttke for access to of London 1926: 533–579. the original specimens housed at Freiberg and Mainz. Florian Witz- Bystrow, A. P. 1935. Morphologische Untersuchungen der Deckkno- mann, Ralf Werneburg, Jrgen Boy, Robert Carroll, and Hans Larsson chen des Schdels der Wirbeltiere, 1. Mitteilung: Schdel der Ste- are thanked for helpful discussions. Jrg Frbisch read earlier versions gocephalen. – Acta Zoologica 16: 65–141. of the manuscript and we thank him for his constructive suggestions. Clausing, A., & Boy, J. A. 2000. Lamination and primary production This project was funded by a graduate student award to NBF through in fossil lakes: relationship to palaeoclimate in the Carboniferous- a NSERC discovery grant to R. L. Carroll, McGill Graduate Student Permian transition. In Hart, M. B. (ed.). Climates: Past and Pre- Fellowships, and the DFG grant ‘Amphibien-Metamorphose’ to RRS. sent. Geological Society, London: pp. 5–16. Credner, H. 1881. Die Stegocephalen (Labyrinthodonten) aus dem Rothliegenden des Plauenschen Grundes. 2. Theil. – Zeitschrift References der Deutschen geologischen Gesellschaft 33: 298–330. Daly, E. 1994. The Amphibamidae (Amphibia: ), with Ammon, L. von 1889. Die permischen Amphibien der Rheinpfalz. a description of a new genus from the Upper Pennsylvanian of Straub, Mnchen. Kansas. – The University of Kansas Miscellaneous Publica- Anderson, J. D. 1971. The life history and systematics of Ambystoma tions 85: 1–59. rosaceum. – Copeia 4: 371–377. Denoel, M., Hervant, F., Schabetsberger, R. & Joly, P. 2002. Short- Anderson, J. S., Reisz, R. R., Scott, D., Frbisch, N. B. & Sumida, and long-term advantages of an alternative ontogenetic pathway. S. S. 2008. A stem batrachian from the Early Permian of Texas – Biological Journal of the Linnean Society 77: 105–112. and the origin of frogs and salamanders. – Nature 453: 515–518. Duellman, W. E., & Trueb, L. 1986. Biology of amphibians. McGraw- Becq-Giraudon, J.-F., Montenat, C., & Van den Driessche, J. 1996. Hill Book Co., New York. Hercynian high-altitude phenomenan the French Massif Centrale: Frbisch, N. B., Carroll, R. L. & Schoch, R. R. 2007. Limb ossifica- tectonic implications. – Paleogeography, Paleoclimatology, Pa- tion in the Paleozoic branchiosaurid Apateon (Temnospondyli) leoecology 122: 127–141. and the early evolution of preaxial dominance in limb Bolt, J. R. 1974. Evolution and functional interpretation of some su- development. – Evolution & Development 9 (1): 69–75. ture patterns in Paleozoic labyrinthodont amphibians and lower Green, J. 1825. Description of a new species of salamander. – Journal . – Journal of Paleontology 48: 434–458. of the Academy of Natural Sciences Philadelphia 5: 116. Boy, J. A. 1971. Zur Problematik der Branchiosaurier (Amphibia, Kar- Harris, R. N. 1987. Density-dependent paedomorphosis in the sala- bon – Perm). – Palontologische Zeitschrift 45 (3/4): 107–119. mander Notophthalmus viridescens dorsalis. – Ecology 68 (3): Boy, J. A. 1972. Die Branchiosaurier (Amphibia) des saarpfaelzischen 705–712. Rotliegenden (Perm, SW-Deutschland). – Abhandlungen des hes- Harris, R. N. 1989. Ontogenetic change in size and shape of the facu- sischen Landesamt fr Bodenforschung 65: 6–137. latively paedomorphic salamander Notophthalmus viridescens. – Boy, J. A. 1974. Die Larven der rhachitomen Amphibien (Amphibia: Copeia 1989 (1): 35–42. Temnospondyli; Karbon-Trias). – Palontologische Zeitschrift 48: Harris, R. N., Semlitsch, R. D., Wilbur, H. M. & Fauth, J. E. 1990. 236–268. Local variation in the genetic basis of paedomorphosis in the sala- Boy, J. A. 1978. Die Tetrapodenfauna (Amphibia, Reptilia) des saarpfl- mander Ambystoma talpoideum. – Evolution 44 (6): 1588–1630. zischen Rotliegenden (Unter-Perm; SW-Deutschland). 1. Branchio- Meyer, H. von 1844. Briefliche Mitteilungen and Prof. Bronn. – saurus. – Mainzer geowissenschaftliche Mitteilungen 7: 27–76. Neues Jahrbuch fr Mineralogie, Geognosie, Geologie und Petre- Boy, J. A. 1986. Studien ber die Branchiosauridae (Amphibia: Tem- faktenkunde 1844: 336–337. nospondyli) 1. Neue und wenig bekannte Arten aus dem mittel- Milner, A. R. 1982. Small temnospondyl amphibians from the middle europischen Rotliegenden (?oberstes Karbon bis unteres Perm). Pennsylvanian of Illinois. – Paleontology 25 (3): 635–664. – Palontologische Zeitschrift 60: 131–166. Patterson, K. K. 1978. Life history aspects of paedogenic populations Boy, J. A. 1987. Studien ber die Branchiosauridae (Amphibia: Tem- of the Ambystoma talpoideum. – Co- nospondyli; Ober-Karbon – Unter-Perm. Systematische bersicht. peia 1978 (4): 649–655. – Neues Jahrbuch fr Geologie und Palontologie Abhandlun- Patzowsky, M. E., Smith, L. H., Markwick, P. J., Engberts, C. J. & gen 174 (1): 75–104. Gyllenhaal, E. D. 1991. Application of the Fujita-Ziegler paleocli- Boy, J. A. 1988. ber einige Vertrteter der (Amphibia: mate model: Early Permian and Late examples. – Pa- Temnospondyli) aus dem europischen (? hchstes leogeography, Paleoclimatology, Paleoecology 86: 67–85.

# 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim museum-fossilrecord.wiley-vch.de 90 Fro¨ bisch, N. B. & Schoch, R. R.: Neoteny in Branchiosauridae

Rafinesque, C. S. 1820. Annals of nature or annual synopsis of new Shaffer, H. B. 1984. Evolution in a paedomorphic lineage. II. Allome- genera and species of animals, plants, etc. discovered in North try and form in the Mexican ambystomatid salamanders. – Evolu- America. Thomas Smith, Lexington (Kentucky). tion 38: 1207–1218. Schoch, R. R. 1992. Comparative ontogeny of early Permian bran- Shaffer, H. B. & Voss, S. R. 1996. Phylogenetic and mechanistic ana- chiosaurid amphibians from southwestern Germany. – Palaeonto- lysis of a developmentally integrated character complex: Alterna- graphica, Abteilung A 222: 43–83. tive life history modes in ambystomatid salamanders. – American Schoch, R. R. 1995. Heterochrony in the development of the amphi- Zoologist 36: 24–35. bian head. In McNamara, K. J. (ed.). Evolutionary change and Shaw, G. & Nodder, F. P. 1789. The Naturalist’s Miscellany, or co- heterochrony. John Wiley & Sons Ltd., New York: pp. 107–124. loured figures of natural objects; drawn and described from nat- Schoch, R. R. 1999. Comparative osteology of Mastodonsaurus gigan- ure. Vol. 9. London. teus (Jaeger, 1828) from the Middle (Lettenkeuper: Lon- Snyder, R. C. 1956. Comparative features of the life histories of Am- gobardian) of Germany (Baden-Wrtemberg, Bayern, Thringen). bystoma gracile (Baird) from populations at low and high alti- – Stuttgarter Beitrge zur Naturkunde 278: 1–175. tudes. – Copeia 1: 41–50. Schoch, R. R. 2001. Can metamorphosis be recognized in Paleozoic Sprules, W. G. 1974. The adaptive significance of paedogenesis in amphibians? – Neues Jahrbuch fr Geologie und Palontologie North American species of Ambystoma (Amphibia: Caudata): an Abhandlungen 220 (3): 335–367. hypothesis. – Canadian Journal of Zoology 52 (1974): 393–400. Schoch, R. R. 2002a. The early formation of the skull in extant and Tihen, J. A. 1942. A colony of fossil neotenic A. tigrinum. – Univer- Paleozoic amphibians. – Paleobiology 28 (2): 278–296. sity of Kansas Science Bulletin 28: 189–198. Schoch, R. R. 2002b. The evolution of metamorphosis in temnospon- Werneburg, R. 1988. Die Stegocephalen der Goldlauterer Schichten dyls. – Lethaia 35: 309–327. (Unterrotliegendes, Unterperm), Teil II: Apateon kontheri n. sp., Schoch, R. R. 2004. Skeleton formation in the Branchiosauridae: a Melanerpeton eisfeldi n. sp. des Thringer Waldes und andere. – case study in comparing ontogenetic trajectories. – Journal of Freiberger Forschungshefte C 427: 7–23. Vertebrate Paleontology 24: 309–319. Werneburg, R. 1991. Die Branchiosaurier aus dem Unterrotliegend Schoch, R. R. & Carroll, R. L. 2003. Ontogenetic evidence for the des Dhlener Beckens bei Dresden. – Verffentlichungen des Paleozoic ancestry of salamanders. – Evolution & Develop- Naturhistorischen Museum Schleusingen 6: 75–99. ment 5 (3): 314–324. Werneburg, R. 2002. Apateon dracyiensis – eine frhe Pionierform Schoch, R. R. & Rubidge, B. S. 2005. The amphibamid aus dem europischen Rotliegend, Teil 2: Palokologie. – Verf- from the Lystrosaurus Assemblage Zone of South Africa. – Jour- fentlichungen des Naturhistorischen Museum Schleusingen 17: nal of Vertebrate Paleontology 25 (3): 502–522. 17–32. Schoch, R. R. & Frbisch, N. B. 2006. Metamorphosis and neoteny: Werneburg, R. & Schneider, J. W. 2006. Amphibian biostratigraphy of alternative pathways in an extinct amphibian clade. – Evolu- the European Permo-Carboniferous. In Lucas, S. G., Cassinis, G. tion 60 (7): 1467–1475. & Schneider, J. W. (eds). Non-marine Permian Biostratigraphy Schoch, R. R., Fastnacht, M., Fichter, J. & Keller, T. 2007. Anatomy and Biochronology. The Geological Society of London Special and relationships of the Triassic temnospondyl Sclerothorax. – Publications, London 265: 201–215. Acta Palaeontologica Polonica 52: 117–136. West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Schoch, R. R. & Milner, A. R. 2008. The intrarelationships and evolu- Oxford University Press, New York. tionary history of the temnospondyl family Branchiosauridae. – Whiteman, H. 1994. Evolution of facultative paedomorphosis in sala- Systematic Palaeontology 6 (4): 409–431. manders. – The Quarterly Review of Biology 69 (2): 205–221. Semlitsch, R. D. & Gibbons, J. W. 1985. Phenotypic variation in meta- Wiens, J. J., Bonett, R. M. & Chippindale, P. T. 2005. Ontogeny dis- morphosis and paedomorphosis in the salamander Ambystoma tal- combobulates phylogeny. – Systematic Biology 54 (5): 91–110. poideum. – Ecology 66 (4): 1123–1130. Wilbur, H. M. & Collins, J. P. 1973. Ecological aspects of amphibian Semlitsch, R. D., Harris, R. N. & Wilbur, H. M. 1990. Paedomorpho- metamorphosis. – Science 182: 1305–1314. sis in Ambystoma talpoideum: Maintanance of population varia- Witzmann, F. & Schoch R. R. 2006. The postcranium of Archego- tion and alternative life-history pathways. – Evolution 44 (6): saurus decheni, and a phylogenetic analysis of temnospondyl 1604–1613. postcrania. – Palaeontology 49: 1211–1235.

museum-fossilrecord.wiley-vch.de # 2009 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim