The evolution of life cycles forms the subject of numerous studies on extant organisms, but is rarely documented in the fossil record. Here, I analyze patterns of development in time-averaged samples of late Carboniferous and early Permian amphibians, and compare them to paleoecological patterns derived from the same deposits located within a large sedimentary basin (Saar-Nahe, Germany). In 300-297 million years (myr) old Sclerocephalus haeuseri (1–1.7 m), adult size, morphology, and the course of ontogeny varied with respect to the habitats in which the species existed. These differences are best exemplified by ontogenetic trajectories, which reveal a full range of modifications correlating with environmental parameters (lake properties, food resources, competitors). In a 2- to 3-myr-long interval, six different lake habitats were inhabited by this species, which responded to changes by modification of growth rate, adult size, developmental sequence, skeletal features, prey preference, and relative degree of terrestriality.
The evolution of life cycles continues to receive increasing attention. One recently successful field is the study of body plan formation in early development and the analysis of how patterns of evo–devo relate to paleontological evidence (Shubin et al. 2009). This has revealed fascinating insights into deep homology (Coates and Clack 1990; Shubin et al. 1997; Clack 2009). A second major aspect is the evolutionary interplay between ontogeny and the environment, a research program still largely restricted to recent organisms (Schlichting and Pigliucci 1998; West-Eberhard 2003). For paleontology to contribute substantially to this field, preservation has to be exceptionally good, specimen numbers need to be unusually high, and localities are to be studied in great detail by experts from different fields (sedimentology, taphonomy, paleoecology). Even if these rare conditions are met, they are mostly restricted to one locality and horizon; yet to study evolutionary changes, a sequence of different horizons with a sufficient, but not too wide stratigraphic distance is required.
Extremely rich samples of fossil amphibians have been excavated in the Saar-Nahe Basin of southwestern Germany (Boy and Sues 2000). The often-complete skeletons are preserved in Paleozoic mudstones and carbonates that are formed in intermontane lakes (Boy and Sues 2000), and have often conserved skin impressions, gut contents, and stains of external gills. Ever since their first discovery, the exquisitely preserved amphibians attracted the attention of paleontologists (Meyer 1844, 1858; Broili 1926; Bulman and Whittard 1926; Boy 1972, 1987, 2007). It is predominantly material from these deposits that has contributed detailed information on the ontogeny of fossil amphibians (Boy 1974; Schoch 1992; Boy 1995; Boy and Sues 2000; Schoch 2003, 2004; Witzmann 2006). Recently, excavations at numerous localities have yielded significant data on the sedimentology of the lakes (Boy 1987), their faunal content (Schindler and Heidtke 2007), and their paleoecology (Boy 1998, 2003). Although these data have been collected and published, they have not been analyzed with respect to the rich ontogenetic data available from the amphibians found in the same localities. Preservation, sample sizes, and spatiotemporal distribution of successive lake horizons all meet the conditions required for analyzing patterns of developmental evolution in the preserved amphibian species.
The objective of this article is (1) to analyze patterns of development in these late Paleozoic amphibians at the species and (time-averaged) population levels, and (2) to calibrate them with stratigraphic, sedimentological, and paleoecological data. The major aim is to document microevolutionary changes with a particular focus on the interplay of developmental evolution and ecology, by addressing both intrinsic (ontogenetic) and extrinsic (ecological) aspects of microevolution in a long-extinct clade of amphibians. The taxon selected for study is Sclerocephalus haeuseriGoldfuss 1847, a well-known 1–1.7 m long fish predator (Boy 1988; Schoch 2003; Schoch and Witzmann 2009).
Material from six different lake deposits provided sufficient data for reconstructing the ontogenetic trajectories of S. haeuseri. The material was collected mostly during scientific excavations, supplemented by material acquired by private collectors and numerous data on material published by Krätschmer (2006). These excavations focused on well-known horizons (Boy 1987) and only finds of unequivocal provenance and stratigraphical age were studied.
The material is housed in the following institutions (number of studied specimens given in brackets): Bayerische Staatssammlung für Paläontologie Munich (5), Bundesanstalt für Geologie und Rohstoffe Berlin-Spandau (4), Eberhard-Karls-Universität Tübingen (5), Geoskop Thallichtenberg (38), Haus der Natur Salzburg (1), Johannes-Gutenberg-Universität Mainz (28), Musée d'Histoire Naturelle Fribourg (1), Museum für Naturkunde Berlin (26), Museum der Saarbergwerke Saarbrücken (13), Museum Stapf Nierstein (8), Naturhistorisches Museum Mainz (8), Naturmuseum Senckenberg Frankfurt (2), Natural History Museum Tokyo (1), Staatliches Museum für Naturkunde Karlsruhe (6), Staatliches Museum für Naturkunde Stuttgart (22).
I analyzed specimens from six different lake deposits encompassing four different time intervals (Fig. 1). These water bodies differed substantially in size, duration, and biotic properties (Boy 1987, 1994; Boy and Sues 2000; Schindler 2007). During the Carboniferous-Permian boundary, the Saar-Nahe Basin formed a 120-km-long, SW-NE stretching intermontane depression (Fig. 1, left). This depression was situated in the central part of a large mountain range, the Variscan Orogen. The Saar-Nahe Basin was affected by various tectonic faults, one of which subdivided the basin into a northern and a southern part (Schäfer 1989). Depending on the size and depth of the lakes, this subdivision had an impact on some, but not all water bodies existing during that time interval (Fig. 1, right). The geomorphological setting appears to have remained the same throughout the studied time period, which is represented by the upper part of the Meisenheim Formation (Lower Rotliegend), spanning some 1–2 million years (Schindler 2007).
The following lakes have been identified (Boy 1987, with stratigraphical levels referred to as M6–10): (1) M6, in which a medium-sized water body (Lake Jeckenbach) existed in the northern part (30 km length) and a much smaller one (Lake Niederkirchen) in the southern part (10 km); (2) M8, during which the two subbasins were flooded by a larger lake (Lake Odernheim) that covered almost half of the Saar-Nahe Basin area (40 km); (3) M9, in which a large lake existed in the northern part (Lake Kappeln, 70 km long) and a smaller lake in the southern region (Lake Pfarrwald, 20 km); and finally M 10, during which almost the entire Saar-Nahe Basin was covered by a deep, long-lived water body (Lake Humberg-Lebach) approaching 80 km length (Fig. 1).
Boy and coworkers (Boy 1972, 1987; Boy et al. 1990; Boy 1998, 2003) collected rich data on the paleoecology of the aforementioned lakes. These include (1) numerous sedimentological and geochemical data, (2) analysis of co-occurring algae, plants, and invertebrates, and (3) analysis of fossil feces (coprolites) and intestinal fillings in well-preserved skeletons. In most cases, the large samples of vertebrates come from a few rich beds, such as carbonate layers and concretions (Jeckenbach, Odernheim, Kappeln) or paper shale and black shale mudstones (Niederkirchen, Pfarrwald, Humberg). The fauna from these lake deposits is autochtonous; in addition, there is no evidence of size selection between the time of death and final deposition of the recovered vertebrates (Boy 2003). This is highlighted by the frequency distribution of specimens assessed for each lake (Fig. 2). These data permitted the study of lake paleo-ecosystems, although the preserved fauna is only a fraction of the original biota, because most of the plankton, soft-bodied invertebrates, and early larvae of fish and amphibians had little potential for preservation (Boy 2003).
The studied beds are likely to have formed in a rather short period of geological time (101–103 years). However, even in such beds, natural populations cannot be studied directly. In a few cases, so-called “census populations” were preserved, representing mass deaths caused by some catastrophic event (e.g., algal blooms and subsequent poisoning, one likely factor discussed by Boy 2003). Census populations are known from Lake Odernheim, where some carbonate beds yield hundreds of palaeonisciform fish and small amphibians on single-bedding planes. The most likely cause is seasonal algal blooms. Usually, these single layers cannot be followed over more than a few meters laterally simply because the rocks do not split accordingly. In the much more common case, populations were time-averaged over several hundreds of years, giving a cross-section of the population over a longer period of time, the so-called “normal population” (Dodd and Stanton 1992). These are the samples studied in the present article, and to highlight their difference to modern samples I refer to them as “populations.”
SAMPLES, SIZE RANGES, AND LAKE HABITATS
The temnospondyl amphibian S. haeuseri was the largest aquatic predator in the Saar-Nahe Basin. It had a long and heavy parabolic skull, strong teeth, and an elongate body with a high swimming tail. Due to more than a hundred specimens housed in public collections, this taxon forms one of the best-known early amphibians, indeed lower tetrapods (Boy 1988; Schoch and Witzmann 2009). The early ontogeny of the species is known in great detail, preserving numerous ontogenetic phases in which bones were formed successively (Boy 1988; Schoch 2003; Witzmann 2006). Based on this source of data, an ontogenetic trajectory could be reconstructed (see next section).
In the present study, only published material and new specimens available in public collections were considered (Broili 1926; Boy 1988; Schoch 2003; Krätschmer 2006; Schoch and Witzmann 2009). On this basis, the size ranges of “populations” were calculated for each lake, mapped onto the histograms of Figure 2. Not all of these specimens were preserved well enough and in the required state of articulation to permit assessment of the developmental state. Specimens for which this was possible are mapped onto the diagram B in Figure 3, with numbers of specimens defining a given size range provided. This diagram shows that there is substantial evidence for the existence of divergent ontogenetic trajectories (reconstructed in diagram A of the same figure), despite broad variation of some events within a given “population.” Many additional specimens are kept in private collections. Some of these have been seen by the author but were not included in the present study; their inclusion would not change the recognized patterns, however.
These analyzed samples indicate that S. haeuseri (in the following only referred to by its genus name) was breeding in all six studied lakes (Fig. 2). In all these deposits, Sclerocephalus larvae are abundant and adult size classes are also present. Further, it is known that Sclerocephalus preyed in all these environments on palaeonisciform actinopterygians. In five lakes, this was the genus Paramblypterus, whereas in Lake Niederkirchen it was its distant relative Aeduella (Boy and Sues 2000). In all deposits, specimens of Sclerocephalus were found with intestinal fillings that predominantly contained either of these two fish genera. In one of these deposits (Lake Kappeln), large specimens of Sclerocephalus contain juveniles of the same species, indicating that some adults of this “population” were occasionally cannibalistic.
The frequency of Sclerocephalus clearly differs between these lakes, with the Jeckenbach and Kappeln deposits having produced the largest quantities of specimens, and the Pfarrwald and Niederkirchen localities the smallest samples (Fig. 2). The conclusion that Sclerocephalus inhabited all these lakes and raised its young there is drawn from the preserved size distribution, which includes all size classes, irrespective of total specimen number. If Sclerocephalus had bred elsewhere, larvae and juveniles should not be present in the observed quantities.
A general pattern of all lakes is that larvae form the most frequent size classes and large adults the least frequent, which is consistent with observations in other lake deposits (Boy and Sues 2000). However, the absolute quantities differ substantially, as well. For instance, in the Jeckenbach Lake juveniles and early adults were relatively more abundant, and this lake also yielded the largest number of adults. In four lakes (Jeckenbach, Niederkirchen, Kappeln, and Pfarrwald), Sclerocephalus reached very large size (180–250 mm skull length), approaching 1.5–1.7 m body length. Conversely, in Lakes Odernheim and Humberg, which have produced substantial quantities of specimens, adults did not exceed 125–130 mm skull length (1.2 m body length). These two lakes were also the largest and longest-lasting water bodies, spanning some 70–80 km in their long axes (Fig. 1).
To sum up, Sclerocephalus was native to all six studied lakes and was selective of prey (mostly palaeonisciforms), but reached different adult sizes in these various environments. In addition, adult morphology and developmental patterns were quite different in the six “populations” (=time-averaged or normal populations) of Sclerocephalus. The morphological diversity is only apparent when large adults are compared, while the developmental differences are best studied by the analysis of ontogenetic trajectories.
VARIATION IN ONTOGENY AND MORPHOLOGY
Numerous ontogenetic data supplement the observations on size and frequency depicted in Figure 2, and reveal subtle differences between the time-averaged “populations” of the six lake deposits. These data indicate that, depending on the lake habitats, Sclerocephalus employed different growth strategies and that its development followed divergent ontogenetic trajectories. In the present study, the well-known developmental sequence of S. haeuseri from Lake Jeckenbach forms the standard trajectory (Fig. 3, bold black line). This deposit forms a large sample and shows the most even representation of size classes. In Lake Jeckenbach, Sclerocephalus grew to large adult size and eventually developed skeletal features typical of amphibious tetrapods capable of making occasional excursions on land (see Fig. 3A, inset skeleton figure, and Schoch and Witzmann 2009). Still, it is not likely that any of the studied Sclerocephalus“populations” produced entirely terrestrial adults. This is obvious when Sclerocephalus is compared with fully terrestrial “upland” dwellers, the dissorophoids or seymouriids (Schoch 2009). However, in two lakes (Niederkirchen, Kappeln) Sclerocephalus apparently left the habitat as adult to lead a more amphibious life, possibly at the shore, which probably involved frequent land excursions.
The ontogenetic trajectory of Jeckenbach Sclerocephalus includes the following major phases: (1) formation of dermal skull bones, neural arches, ribs, and limb elements (Schoch 2003); (2) ossification of stapes and ischium, (3) incipient formation of vertebral centra and jaw articulation (Witzmann 2006), and finally (4) ossification of braincase and the completion of limb and girdle skeletons (Schoch and Witzmann 2009). The single events that make up the trajectory are listed on the y-axis in Figure 3, and their sequence was identical throughout the studied “populations.” This means that there were no sequential heterochronic events in the evolution of these “populations.” In the following, I will make some comparisons involving the rate at which developmental events succeeded in the different trajectories; these statements are always based on the hypothetical correlation of (unknown) individual age with body size. Although body size may often not strictly correlate with age, new data on branchiosaurids from the same lake deposits indicate that size and skeletochronological age match quite well in these cases (Sanchez et al., in press).
The reported trajectory does only hold for specimens collected at the Jeckenbach locality, (horizon M6, Lake Jeckenbach). At two other sites within the same horizon and lake deposit, indeed the same sedimentary facies, development of Sclerocephalus followed slightly divergent trajectories. At Rehborn, ossification of the carpals and tarsals proceeded more rapidly as measured by size, while the pubis was still cartilaginous in the largest specimens. More substantial differences were found at Raumbach, where the braincase and central limb elements started to form earlier and proceeded more rapidly with completion. This variation is reflected by the relatively broad ranges of later developmental events in Figure 3B.
In Lake Niederkirchen, which was roughly coeval with Lake Jeckenbach but had a geographically isolated fauna, Sclerocephalus is too rare to provide evidence for a complete ontogenetic trajectory (Fig. 2); the known developmental stages parallel those of Lake Kappeln rather than Lake Jeckenbach, and the adult morphology is most similar to Sclerocephalus from Lake Kappeln, as well: the skull lacked tabular horns, the orbits were small and widely separate, and the limbs were extremely stout and robust.
In Lake Odernheim, Sclerocephalus reached only small adult size. Most of the developmental events typical of late juvenile and adult phases of the trajectory were not reached, and the cranial morphology was quite different: ornament radial with long ridges and deep lateral line sulci present even in adults. The lateral line is usually found in larvae of other Sclerocephalus“populations”—its retention in Odernheim Sclerocephalus could indicate the dominance of the lateral sense in prey localization, possibly reflecting life in deeper water. The elongated swimming tail in adults (100–130 mm skull length) also suggests a fully aquatic mode of life.
In the next time slice, Lakes Kappeln and Pfarrwald were again roughly coeval and completely separated geographically. Lake Pfarrwald yielded few specimens but still a partial ontogenetic trajectory could be reconstructed, departing in several points from the standard Jeckenbach trajectory (Fig. 3): the quadrate and exoccipital formed earlier and the ossification of the skull proceeded at a faster pace, teeth were larger, with conspicuous differences in the ornament, as well. In Lake Kappeln, Sclerocephalus developed at an intermediate pace in the juvenile phase (faster than Jeckenbach and more slowly than Pfarrwald “populations”), but in the early adult phase it differs by starting ossification of the central limb bones. Morphologically, Kappeln and Pfarrwald Sclerocephalus form extreme end points: although the Kappeln “population” became ever more short-bodied with growth and had proportionately large limbs, the Pfarrwald morph had a long trunk that became even relatively longer in large adults.
In Lake Humberg-Lebach, Sclerocephalus did not reach the large size of most previous “populations” and its ontogenetic trajectory was much shorter than that of the Jeckenbach, Kappeln, and Pfarrwald morphs. However, in contrast with Lake Odernheim, Humberg Sclerocephalus does not essentially differ morphologically from the Kappeln form, only that because of the smaller adult size it is less robustly ossified, and it retained the long swimming tail and lateral line sulci like the Odernheim morph.
ENVIRONMENT, ONTOGENY, AND MICROEVOLUTION
The reported differences in ontogeny and morphology correlate with certain properties of the lake deposits. Together, these data provide evidence for evolutionary modifications of life histories in Sclerocephalus as a response to divergent lake habitats. In the following, I will only synthesize the main data that support hypotheses of why development and morphology differ between the “populations” of Sclerocephalus; a complete list of paleoecological and morphological data supporting these conclusions is given in Figure 4.
In the stratigraphically oldest deposits yielding S. haeuseri, this species preferred small lakes and was generally rare (e.g., Lake Concordia near St. Wendel). The presence of larvae suggests that it was breeding there, but sometimes it may have preferred other habitats (not necessarily terrestrial) as an adult. The largest specimens did not exceed 130 mm skull length (Broili 1926; Boy 1987). It is unclear whether these habits form the primitive condition of Sclerocephalus, but a close morphological resemblance of these oldest samples to that of Lake Jeckenbach indicates that the Jeckenbach sample may at least form a model for the primitive condition of the evolutionary sequence to be studied here.
1At the small Lake Niederkirchen, Sclerocephalus was only present in a short early phase, and probably left the water as adult, returning during the breeding season. The main limiting factor was the presence of a large top predator (the shark Orthacanthus), which preyed on the same fish as Sclerocephalus and had inhabited the lake before Sclerocephalus appeared there (Boy 1998). At Niederkirchen, the heavy postcranial skeleton and short tail of adult Sclerocephalus indicate that it was able to leave the water within a size range at which Orthacanthus became a serious competitor.
2At Lake Jeckenbach, Sclerocephalus was relatively common and remained in the same habitat throughout its life. This lake was larger than most previous ones, moderately deep and long-lived, and rich in resources (Boy 1987; Schindler 2007). It sometimes possessed an euxinic bottom zone and a stable upper layer, which allowed palaeonisciforms (Paramblypterus) to be abundant and reach a large body size. Sclerocephalus was present in the most stable and ecologically diverse phase of the lake, preying on Paramblypterus. The main factors for the large size and permanent presence of Sclerocephalus appear to have been (a) the rich food resources and (b) the absence of large competitors. Apparently, most Jeckenbach “populations” of Sclerocephalus remained in the lake as adults, where they reached large size and had a heavily ossified skeleton, while retaining lateral lines and a relatively long swimming tail. The only partial food competitor was the 1-m-long rhipidistian Ectosteorhachis, which probably focused on smaller fish than adult Sclerocephalus.
3Lake Odernheim was shallower and larger, but as rich in resources as Lake Jeckenbach (Boy 1972). However, it housed an impoverished fauna consisting of a single palaeonisciform (Paramblypterus) and the amphibians Apateon pedestris, Micromelerpeton credneri, and Sclerocephalus. All taxa attained significantly smaller adult sizes compared to other lakes. The tiny amphibians were extremely common (in some beds forming census populations) whereas the fish and Sclerocephalus were less abundant, which indicates unstable conditions, because branchiosaurids were the most flexible vertebrates in these lakes (Boy and Sues 2000). Boy (2003) reported further evidence for high levels of environmental stress probably caused by seasonal fluctuations: algal blooms and rhythmic circulation caused mass deaths of branchiosaurids and fish, which cover single layers in large quantities. These less favorable conditions appear to have formed the limiting factor, with Sclerocephalus truncating development and reaching smaller adult size compared to the Jeckenbach sample. Morphologically, Sclerocephalus retained lateral lines as an adult and failed to form crucial bones in both the skull and postcranium (Figs. 3 and 4). The overall ossification in the skeleton (bone thickness) was much less extensive than in the Jeckenbach sample. It is unlikely that Sclerocephalus simply left the lake in later life, because despite the substantial sample, not a single larger specimen was found. In addition, the elongated snout of the largest specimens (130 mm skull length) indicates that these specimens were fully mature, a stage reached by Jeckenbach “populations” only well beyond 200 mm.
4Lake Kappeln was larger than all previous water bodies in the basin, but probably not substantially deeper than Lake Odernheim (Schindler 2007). It was accessed by rivers in some periods, then permitting benthos to exist. Its fauna was most similar to that of Lake Jeckenbach (Boy 1987). Sclerocephalus grew to similar adult size as in Lake Jeckenbach; and larvae, juveniles, and early adults were abundant. Despite general morphological similarity, the short trunk and tail, heavy ribs, and extremely robust limbs of Kappeln Sclerocephalus show that adults of this sample were the most terrestrial of all studied samples—the largest, Eryops-like adult was even granted a distinct species name (see discussion in Schoch and Witzmann 2009), but the question whether the Kappeln “population” originated by a speciation event is not relevant here. The preserved size classes suggest that Kappeln Sclerocephalus was native to the lake up to 130 mm skull length, thereafter becoming rare, which forms a stark contrast to the situation in Lake Jeckenbach (Fig. 2). In Lake Kappeln, this correlates with the presence of a second taxon (Cheliderpeton lellbachae, see Krätschmer 2006), which was clearly more aquatic (long trunk, very long swimming tail, longer snout, lateral lines) and remained in the lake as adult (up to 160 mm skull length). These facts indicate that the ecosystem did not permit the coexistence of two large adult predators (with adult Sclerocephalus consequently leaving the lake), although larvae and juveniles of the two co-occurred and fed on juveniles of the same palaeonisciform fish (Paramblypterus). Another observation reveals that Sclerocephalus was cannibalistic in this lake, a phenomenon found in unstable environments or during periods of food shortage (Elgar and Crespi 1992). Hence, competition among large fish predators appears to have been the main factor in Lake Kappeln, with cannibalism and change of habitat forming two results. Adult Sclerocephalus changed to a probably more terrestrial habitat (lake shore?) but returned during the breeding season, when it was occasionally preserved. In contrast to the Jeckenbach “population,” Kappeln Sclerocephalus had crucial events for establishing a terrestrial tetrapod occur earlier (relative to skull length), and the trajectory was extended (in comparison to that of Lake Jeckenbach) to complete ossification of the pelvic girdle, a feature correlating with terrestrial locomotion.
5Lake Pfarrwald was generally similar to lake Jeckenbach in size, facies, and trophic system (Boy 1987; Schindler 2007), but existed at roughly the same time as Lake Kappeln, from which it was completely separated. A major difference to Lakes Jeckenbach and Kappeln was the isolation from water influx, which did not permit benthos to settle. At Lake Pfarrwald, Sclerocephalus was more common than at Lake Niederkirchen and present throughout the lifespan of the lake, there forming the only large predator. (Collecting at Lake Pfarrwald was never as focused as in other deposits, therefore the smaller sample size of Sclerocephalus should not be used as a distinction from Lake Jeckenbach). In contrast to Lakes Niederkirchen and Kappeln, the absence of large competitors probably permitted Sclerocephalus to permanently settle in the lake and remain there with its adults. Like in Lake Jeckenbach, Pfarrwald adults had elongated trunks and tails, which generated propulsion in swimming by lateral undulations. Unique features of Pfarrwald Sclerocephalus are that the jaw articulation formed early in development and teeth were relatively larger than in other lakes. Probably Sclerocephalus started to feed on fish earlier than in other lakes (suggested by preserved prey), and therefore developed stronger jaws and larger teeth as juvenile; this coincides with the permanent presence of a smaller carnivore, the branchiosaurid Apateon caducus (Boy 1987), which was feeding on its filter-feeding relative A. pedestris, a tiny aquatic tetrapod that also formed a likely prey for Sclerocephalus larvae. The altered early part of the Pfarrwald trajectory may therefore reflect an escape from a small-sized competitor, while adults formed the single large predators.
6Of all lakes in the Saar-Nahe Basin, Lake Humberg-Lebach was the largest and also reached the greatest depth (Schindler 2007). Sclerocephalus inhabited this lake only in the earliest phase (Boy 1994), but it was present both at the extrembe eastern and western ends. Similar to Lake Odernheim, Sclerocephalus remained in this lake as an adult, but it did not reach the large body size compared to other lakes. Like Odernheim Sclerocephalus, maximum adult size was in the 120–130 mm range of skull length, although developmentally Humberg Sclerocephalus was more advanced (see Fig. 3A) and its skeleton more robustly ossified than the Odernheim “populations,” which indicates somewhat better living conditions in Lake Humberg. This is supported by the larger size of palaeonisciforms, which still formed the prey of Sclerocephalus. Like in Lake Odernheim, Humberg Sclerocephalus truncated development to form a medium-sized, fully aquatic predator. The limiting factor was probably also seasonal instability caused by algal blooms (Boy 1994).
PHYLOGENY AND STRATIGRAPHY
It is, of course, impossible to say which Sclerocephalus“population” was directly ancestral to which other, or whether there were repeated events of immigration rather than true microevolutionary sequences. Although parsimonious reasoning may suggest ancestor–descendant lineages from the Jeckenbach through Humberg “populations,” the preserved changes in morphology and development appear to have been fluctuating rather than directed. For instance, Jeckenbach and Pfarrwald Sclerocephalus are morphologically quite similar (as are the lake deposits) but they show developmental differences, whereas adults of Niederkirchen and Kappeln Sclerocephalus were similar in different aspects (cranial morphology, limbs), despite major differences between their lake deposits. Further, Odernheim and Humberg Sclerocephalus were similar in the truncation of ontogenetic trajectories, the reduced adult size, and the large size of the lakes they inhabited, but their morphology differed considerably.
Although the lakes succeeded another, they did not form continuous water bodies in time; thus Sclerocephalus and the other vertebrates either immigrated from neighboring habitats (other lakes or rivers), or persisted in transitional lakes of reduced size (still unknown at present). It is probable that S. haeuseri formed a complicated spatiotemporal assemblage of real populations, only some of which are preserved as time-averaged samples (the here studied “populations”), with the interconnecting samples largely lacking. Boy (1988) found evidence of morphological changes and the increase in variablity in Sclerocephalus from M9 and M10, but there was no clear-cut trend either.
PATTERNS OF DEVELOPMENTAL EVOLUTION
Rather than providing evidence for a detailed microevolutionary sequence, the present data document a different kind of pattern: the fine-scale evolution of development and the potential origin of developmental plasticity. The differences in developmental, morphological, and ecological features indicate a high level of evolutionary flexibility in S. haeuseri, both between “populations” and within. For instance, the developmental differences in samples from Lake Jeckenbach (Jeckenbach, Rehborn, Raumbach) suggest a high level of intraspecific developmental and phenotypic plasticity. These three localities, which are only a few kilometers apart, yielded Sclerocephalus with slightly different ontogenetic trajectories and divergent adult morphologies while reaching the same adult size (200–250 mm skull length). At Raumbach, Sclerocephalus had a shorter trunk and tail and acquired a more robust limb skeleton, contrasted by Jeckenbach and Rehborn, where ossification progressed more slowly and the body was more elongated. This could indicate developmental plasticity within one large “population” as a response to slightly variable parameters, but might also form a geographic cline of genetically different “populations.” In the present case, it is impossible to know for certain whether coeval “populations” belonged to the same biospecies, and from a typological perspective even the three different samples from Lake Jeckenbach (Raumbach, Jeckenbach, and Rehborn) might form distinct species. However, from an ecological perspective this makes little sense, especially when the continuity of the habitat and identical food preference can be demonstrated: the three places form closely located sites in the same lake, and the same prey species was found in Sclerocephalus specimens of all three localities. Thus, it is more plausible that Sclerocephalus responded to slight local differences in environmental parameters by a modification of its ontogenetic trajectory, resulting in morphological differences in limb size and robustness, trunk length, and tail length. The correlation between differences in trajectories and functional-adaptive traits indeed indicates that development was subject to evolutionary adjustment. The question remains whether this provides evidence for a broad reaction norm in Jeckenbach Sclerocephalus, or whether the three samples form truly separated populations or demes isolated by some unknown barrier. Both scenarios are plausible, but at present there is no way to decide between them.
The diversity in development and morphology between Sclerocephalus“populations” of different lakes is probably evidence of another kind of evolutionary pattern. As these “populations” were either separated geographically or existed at different times, they did not form a continuous gene pool. Hence, the reported differences exist between entire “populations” rather than within them as might have been the case in Lake Jeckenbach, and the plasticity of development and morphology is not a result of a broad reaction norm. Instead, the differences reveal true microevolutionary changes in development, although we do not know whether intermediate “populations” are absent due to gaps in the fossil record or simply did not exist. Therefore, an assessment of the mode of evolution—gradualism or punctuation, for instance—is not in the reach of the present study. In other words, the exact sequence of changes cannot be studied, but there is sufficient evidence for the existence of microevolutionary change, which by itself reveals the capacity of S. haeuseri to respond (by evolution) to environmental parameters by (evolutionary) modification of its developmental trajectory. As a whole, these data form the most detailed and clear-cut body of evidence for microevolutionary changes in ontogeny in an extinct amphibian species and its potential adaptive background.
In the last decade, ontogenetic data on ever more Paleozoic amphibians have revealed that these animals did not undergo a drastic metamorphosis as modern frogs and salamanders do (Schoch 2001, 2002, 2009). Instead, development progressed slowly with gradual morphological changes. With the exception of a few terrestrial taxa that underwent a fast and profound transformation (Schoch and Fröbisch 2006), many Paleozoic amphibians developed just about sufficient skeletal features to allow them land excursions. The very sluggish tracks ascribed to genera like Sclerocephalus confirm that (Voigt 2007), and it is likely that the more terrestrial “populations” of this taxon lived along the shore of lakes and rivers rather than in remote upland habitats. The large majority of these amphibians fed on fish and spent most of their life in water, such as the giant Mesozoic stereospondyls, which reached sizes beyond 5 m. Developmental plasticity might have been a means to adjust to unstable environmental conditions effectively, as the data on Jeckenbach Sclerocephalus suggest. Developmental evolution was evidently a means to adjust to longer-term changes in environment, or to populate diverse lake habitats. Apparently, the variation between fully aquatic and amphibious adults was readily produced by a slight modification of ontogenetic trajectories; this involved truncation of the sequence and changes in rate rather than sequence changes, which probably became more important in speciations. Such slight modifications could have formed part of the reaction norm of one species (which eventually became narrower or wider in succeeding populations), or alternatively ontogeny evolved in succeeding populations that maintained a narrow reaction norm. In both cases, slight microevolutionary changes in development (or developmental plasticity) could have formed the starting point for long-term evolution, which is normally only observed at a very gross level of the macroevolutionary scale in the fossil record.
Evolutionary biology and paleontology operate on different time scales: the former in terms of generations of natural populations (101–103 years), the latter in terms of sedimentary cycles (105–108 years). Only in very rare cases, namely when preservation is exceptionally good and sedimentation sufficiently fine-scaled and continuous, can the paleontological scale be made finer, reaching even the level of annual cycles. (These cycles are more or less probable to be annual, but this is never certain). However, even in these cases, preserved “populations” are time-averaged and cannot be compared directly with extant populations. Even in the case of continuous sedimentation, preservation potential is not isotropic, which for instance makes a mortality assessment problematic.
Despite the aforementioned, the study of lake deposits, particularly those of long-term water bodies like in the Saar-Nahe Basin, has a bearing on evolutionary biology. In a time window as old as the Carboniferous-Permian boundary, absolute age data are inherently error-laden; notwithstanding many refined results obtained in the last decades, there are principal problems that do not permit a better resolution. Yet these lake deposits, especially when they succeed one another and bear a similar fauna, offer the possibility to study the microevolution of developmental and ecological properties of single species, or at least a set of closely related species. Even though a complete succession of long-extinct populations in time and space is impossible to find in most cases in the fossil record, large samples collected at different stratigraphical levels may still reveal data on patterns of microevolution. Developmental evolution forms a particularly interesting topic in this field, because it links ontogeny with phylogeny, providing evidence on cues by which the internal organismal system responded to environmental parameters. Given that the differences in time scales and terminology of patterns are understood, the evolution of life cycles in Paleozoic amphibians adds interesting data to our understanding of early tetrapod origin and evolution.
Associate Editor: G. Hunt
I thank J.A. Boy, T. Schindler, and F. Witzmann for discussion, K. Krätschmer, M. Manabe, M. Poschmann, A. Schwickert, and H. Stapf for helpful information, and D. Becker, J.A. Boy, O. Hampe, H. Lutz, M. Maisch, W. Munk, M. Nose, M. Rücklin, D. Schweiss, and H. Stapf for access to material. Finally, I want to thank G. Hunt, M. Ruta, and an anonymous referee for their very constructive reviews.