FRFossil RecordFRFoss. Rec.2193-0074Copernicus PublicationsGöttingen, Germany10.5194/fr-21-109-2018A case study of developmental palaeontology in Stereosternum tumidum (Mesosauridae, Parareptilia)Mesosaur developmental palaeontologyBickelmannConstanzehttps://orcid.org/0000-0003-0269-4782TsujiLinda A.linda.tsuji@gmail.comMuseum für Naturkunde, Leibniz-Insitut für Evolutions- und Biodiversitätsforschung, Invalidenstrasse 43, 10115 Berlin, Germany2477 Folkway Drive, Mississauga, ON L5L2J7, CanadaLinda A. Tsuji (linda.tsuji@gmail.com)3April20182111091181November20172February201812February2018This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/This article is available from https://fr.copernicus.org/articles/21/109/2018/fr-21-109-2018.htmlThe full text article is available as a PDF file from https://fr.copernicus.org/articles/21/109/2018/fr-21-109-2018.pdf
Ontogenetic series of extinct taxa are rare. However, if preserved, fossil
embryos and juveniles can provide evidence of developmental plasticity as
related to ecological specialization. Here, we describe articulated and
isolated juvenile material found in close association with an adult
mesosaurid Stereosternum tumidum (MB.R.2089) from Lower Permian
sediments in Brazil, housed in the collection of the Museum für
Naturkunde Berlin. Stylopodial, zeugopodial, and autopodial elements are not
yet completely ossified in the juveniles, as indicated by compression
artifacts on the surface of the bone. These correspond to internal
ossification processes, which have been demonstrated in other aquatic taxa.
Quantitative analysis of measurements in juvenile and adult material reveals
differing growth rates between limb elements: hind limb zeugopodia, which are
massive and elongate in the adult as needed for propulsion, are already
comparatively larger in the juvenile than the humeri, femora, and also the
zeugopodia of the forelimb. This pattern differs from that seen in another
extinct aquatic reptile, Hovasaurus boulei. Nevertheless, we
attribute the accelerated growth rate or earlier onset of ossification to be
a potential developmental pathway generating limb element variation in the
adult present in 280 million year old mesosaurs, which are known for their
fully aquatic lifestyle, in which the hind limbs play a more prominent role
than the forelimbs.
Introduction
The study of fossilized ontogenies is largely confined to postnatal stages
with ossified skeletal elements, due to preservational (taphonomic) factors.
If preserved, they provide valuable insight into the life history of extinct
taxa, as well as evolutionary trajectories. To date, ossification sequences
in fossils are available for some “fish” (Cloutier, 2010), temnospondyl and
lepospondyl amphibians (Fröbisch, 2008; Fröbisch et al., 2010, 2015), “younginiforms” (sensu Bickelmann et al., 2009)
(Currie, 1981; Caldwell, 2002), mosasaurs (Caldwell, 2002), sauropterygians
(Hugi and Scheyer, 2012), ichthyosaurs (Caldwell, 1997), sauropsids (Delfino
and Sánchez-Villagra, 2010) and mammals (Sánchez-Villagra, 2010).
Most of this information is derived from secondarily aquatic taxa, which is
the result of a taphonomic bias (Fröbisch et al., 2010). A notable lack
of published developmental data for early amniote taxa makes each incidence
a valuable contribution to our knowledge of the patterns. Gaining a
comprehensive picture of changes in development and growth in extinct
(fossil) taxa in addition to what we know about development in modern
animals, as approached in this and similar studies, contributes to our
understanding of evolution, developmental trajectories, life history
strategies, and more (Fröbisch et al., 2010).
Overview photographs of rock slab (MB.R.2089.A, a) and latex cast
(MB.R.2089.B, b) of Stereosternumtumidum. For detail (boxes) see Fig. 2.
Scale bar equals 50 mm. For abbreviations see Material and Methods section.
Mesosauridae (Reptilia: Parareptilia) is an extinct secondarily aquatic
group from the Paleozoic; notably, their fossil record also includes
ontogenetic data (Rieppel, 1993; Piñeiro et al., 2012a). The clade
consists of the three monospecific genera Mesosaurus tenuidens, Stereosternum tumidum, and Brazilosaurus sanpauloensis from Lower Permian
localities in Brazil and southern Africa (Oelofsen and Araújo, 1983, 1987).
Their elongate skulls, slender teeth, paddle-like limbs, and thickened
(pachyostotic) trunk ribs are indicative of a secondarily fully aquatic
lifestyle and distinguish mesosaurs from all other Paleozoic amniotes
(Modesto, 2006). Recent studies suggest that mesosaurs, or at least
Mesosaurus, were slow swimmers living in shallow lagoon-like waters, possibly
filter-feeding on pygocephalomorph crustaceans (Piñeiro et al., 2012b;
Villamil et al., 2016). Hypothesized viviparity in Mesosaurus is another potential
indicator of a fully aquatic lifestyle (Piñeiro et al., 2012a). Most
recent studies suggest mesosaurs group basally within parareptiles; a small
amniote clade that originated in the Late Carboniferous (Tsuji and
Müller, 2009; Modesto et al., 2015; though see contradictory hypothesis
of Laurin and Piñeiro, 2017). Evolutionary novelties in this clade
include impedence-matching hearing in nycteroleterids (Müller and Tsuji,
2007), caudal regeneration in mesosaurs (Delfino and Sánchez-Villagra,
2010), derived feeding mechanisms and bipedality in bolosaurids (Reisz et
al., 2007; Berman et al., 2000), and secondarily aquatic lifestyles as well
as (ovo)viviparity in mesosaurids (Modesto, 2006; Piñeiro et al.,
2012a), all of which occurred in parareptiles as early as the Early Permian.
The first occurrence of congenital scoliosis is also reported from members
of this clade (Szczygielski et al., 2017). Fortunately, there is some
ontogenetic data available for parareptiles, such as in the pareiasaurs
Elginia (Spencer and Lee, 2000) and Deltavjatia (Tsuji, 2013), procolophonids (Cisneros,
2008), and Mesosaurus (Rieppel, 1993; Piñeiro et al., 2012a).
Here, we describe a remarkable specimen containing an adult Stereosternum tumidum next to
juvenile material from Lower Permian sediments in Brazil; a specimen long
neglected in the fossil collections at the Museum für Naturkunde Berlin.
Parent–hatchling associations in mesosaurs have thus far only been described
for the sister-taxon Mesosaurus (Piñeiro et al., 2012a). The present finding of
differing developmental stages allows for the establishment of baseline
ossification sequences and growth rates. This study proposes that they
relate to the adaptation of mesosaur limbs to a fully aquatic lifestyle.
Material and Methods
Specimen MB.R.2089 consists of a natural mold (MB.R.2089.A), preserving an
articulated adult postcranium and the articulated postcranial elements of a
juvenile, as well as an isolated long bone from another juvenile (Fig. 1). A
latex cast (MB.R.2089.B) was prepared at the Museum für Naturkunde
Berlin in 2013. In this, the adult is visible in ventral aspect. It was not
until the latex cast was made that the juvenile skeleton was recognized as
such, and the majority of the anatomical observations of this smaller
skeleton were made directly from the cast. A historical label applied to the
specimen assigned the adult to the taxon Stereosternum tumidum, an identification we verify using
the anatomical features listed below. The close proximity of the juvenile
material to the adult on the rock slab strongly suggests kinship
(Piñeiro et al., 2012a).
Systematic Paleontology
Parareptilia Olson, 1947
Mesosauridae Baur, 1889
Stereosternum tumidum Cope, 1885
Type specimen: MB.R.2089
Locality and horizon: Itapetininga, Sao Paolo, Brazil. Passa Dois Group.
Irati Formation. Lower Permian. Artinskian. Permian 2.
Limb measurements of juvenile and adult material (mm). Body
length is measured from the caudal end of the posteriormost cervical
vertebra to the approximate position of the first sacral rib. Abbreviations:
d: distal; Epiph: Epiphyses; p: proximal.
The adult consists of a well-preserved and articulated postcranium including
presacral, sacral, and approximately 23 caudal vertebrae, cervical and
abdominal ribs (generally 5mm thick in the midshaft region), as well as both
complete fore- and hind limbs with pectoral and pelvic girdle (Fig. 1). The
skull is absent (Fig. 1). All observable aspects of the postcranial anatomy
conform to that of Stereosternum tumidum, as described by Modesto
(1999, 2010). Specifically, the unfused intermedium and lateral centrale, the
presence of a pisiform, and a diamond-shaped interclavicle characterize this
specimen as Stereosternum rather than Mesosaurus (Fig. 1;
Modesto, 1999, 2010). The fore- and hind limbs are elongate, characteristic
for the aquatic lifestyle proposed for mesosaurs (Modesto, 2006; Piñeiro
et al., 2012a, b; Villamil et al., 2016). Size and appearances of the fore-
and hind limb stylopodia are similar, although the femora are slightly
shorter. The ratio of the midshaft diameter to total length of the femur is
around 9.2 %, which lies between an earlier erected 11 % in
Stereosternum as compared to around 8 % for
Mesosaurus (Modesto, 1999, 2010). Zeugopodial and autopodial
elements of the hind limbs are wider in the midshaft region and the proximal
epiphyses compared to the ones in the forelimbs (Table 1). All limb
measurements are listed in Table 1.
Detailed stippling of postcranium of an isolated femur (a) and the
mostly articulated juvenile (b), based on the latex cast (MB.R.2089.B).
Adult specimen is in grey. Scale bars both equal 10 mm. For abbreviations
see Material and Methods section.
Description of the juvenile material
The juvenile material preserves one mostly complete individual and an
isolated long bone element. Although there is considerable intraspecific
variation in limb element length and shape in sub-adult mesosaurs (Rossmann
and Maisch, 1999), we believe the isolated element belonging to a second
individual of Stereosternum is most likely a femur based on size and
appearance of the element compared to that of the mainly complete individual
(Fig. 2a; Table 1).
The almost complete individual consists of elements of the postcranium,
including vertebral column, ribs, gastralia, and fore- and hind limbs (Fig. 2b).
The skull is not visible; it may be present in the rock in an
underlying layer, or may have been separated from the postcranial on the
missing counterpart (Fig. 2b). Body size, if measured from the approximate
position of last cervical to first sacral rib, is approximately 30 % of
the size of the adult (Table 1). The taphonomic orientation of the skeleton
cannot be attributed, as the elements are typically in close association but
not completely articulated, but the axis of the skeleton is oriented in the
same direction as in the adult and is “stretched out”, rather than curled
into a foetal position (Fig. 2b). The mostly complete juvenile is located
close to the right hind limb of the adult skeleton and does not appear to
have been greatly disturbed pre or post burial, in contrast to the isolated
femur, which lies close to the adult left forelimb. Although the skeletal
elements are not completely articulated as can be seen in the adult, they
are very closely associated and in their approximate anatomical positions.
Cervical vertebrae, located proximal to the forelimbs, are clearly
diagnosable. However, dorsal and caudal vertebrae are distinguishable due
only to their location in situ (Fig. 2b). While cervical vertebrae are fully
developed, the neural arch and pleurocentra of both dorsal and caudal
vertebrae are not yet fully fused and are preserved in two adjacent lines,
though the lack of definitive anatomy in these bones makes it difficult to
identify any individual element (Fig. 2b). Concerning length, the small
skeleton retains what appears to be an almost complete tail, and at least 25
vertebrae can be recognized (Fig. 2b). Further caudally, vertebral elements
are more difficult to discern, yet there appears to be the continuation of
the outline of the soft parts of the tail with occasional bone fragments
visible. Adult Mesosaurus and Brazilosaurus typically have more than 60 caudal vertebrae (Modesto,
2010), so it is reasonable to conjecture that the caudal vertebrae in this
juvenile Stereosternum numbered more than what can be directly observed here. The ribs
are already diagnostically thickened (pachyostotic; most are 2 mm thick in
the midshaft) in the juvenile and are scattered throughout the thoracic
region (Fig. 2b). Slender gastralia lie in the abdominal region (Fig. 2b).
Identifiable juvenile limb elements preserved in MB.R.2089 include two
humeri, three femora, one indeterminate forelimb zeugopodial element, one
indeterminate hind limb zeugopodial element, and three metatarsals. Due to
the extreme delicacy of the juvenile skeleton, other limb elements may be
preserved but obscured under those we can identify, or not differentiated
enough from the “matrix” to definitively name. In the forelimb, both humeri
do not exhibit characteristics such as the deltopectoral crest,
ectepicondylar groove, entepicondylar foramen, and an enlarged entepicodyle
that are present in the adult (Figs. 1, 2b). Instead, they retain
metaphyseal compression and epiphyseal ridges (Fig. 2b) (sensu Hugi and Scheyer,
2012), indicating low maturity similar to what is seen in pachypleurosaur
juveniles (Hugi and Scheyer, 2012). In the hind limbs, all femora show
reduced ontogenetic compression (sensu Hugi and Scheyer, 2012) compared with the
humeri, yet also lack adult phenotypic features such as patellar groove and
muscle attachment sites for trochanter (Fig. 2a, b). One of either the
fibula or tibia can be identified per side (Fig. 2b, Table 1). Due to the
close association of the zeugopod and the preserved metatarsals, we
hypothesize that tarsals are not yet ossified (Fig. 2b), a condition also
seen in other juvenile mesosaur skeletons (i.e. BSP 1979, fig. 4 from Rossman
and Maisch, 1999). Two faint metatarsals can be identified in the latex cast
(MB.R.2089.B). According to their location, we think these might be the
middle ones (II & III; Fig. 2b, Table 1). On the other side, one
indeterminate metatarsal is preserved (Fig. 2b, Table 1).
Comparison of growth ratios in the limbs of the two distantly
related Stereosternum tumidum (MB.R.2089; this study) and “younginiform” Hovasaurus boulei (sub-adult MNHN
1908-21-8 and adult SAM 6231; after Currie, 1981, table 1).
We calculated growth rates using limb measurements in Table 1. We find that
the juvenile hind limb zeugopod, which is longer in the hind limb as
compared to the forelimb in the adult, is already slightly larger (37.5 %
of the adult size) than all other limb elements (ranging from 26.5 % in
the metatarsal III to 35 % in the forelimb zeugopod), indicating a faster
growth rate or an earlier onset of ossification (Table 2).
Further, we compared the established growth rates in MB.R.2089 to earlier
published limb growth data from another secondarily aquatic reptile,
Hovasaurus boulei from the Upper Permian of Madagascar (Currie, 1981). Hovasaurus is a
“younginiform”
diapsid reptile (sensu Bickelmann et al., 2009), for which, fortunately much
ontogenetic material is available (Currie, 1981). It also displays enlarged
hind limbs compared to the forelimbs, which are potentially useful when
swimming (Currie, 1981). Comparing the ossification of limb elements in
sub-adults and adults of Stereosternum and Hovasaurus, we find that the humerus, forelimb zeugopod,
femur, and metatarsals show growth rates or onsets of ossification to be
comparable (Table 2). However, the growth rate of the hind limb zeugopod is
higher in Stereosternum compared to Hovasaurus (Table 2).
Discussion
The secondarily fully aquatic parareptilian clade Mesosauridae is renowned
for an exceptional fossil record including the preservation of multiple
growth stages, tail regeneration, along with the earliest report of
(ovo)viviparity in amniotes (Rieppel, 1993; Delfino and
Sánchez-Villagra, 2010; Piñeiro et al., 2012a). Here, we describe a
congregation of adult and sub-adult (or potentially hatchling) material of
the taxon Stereosternum tumidum. Parent-hatchling associations have been previously reported in
mesosaurs only in Mesosaurus tenuidens (Piñeiro et al., 2012a).
Ontogenetic series of fossils provide valuable insights into life history
traits of organisms (Fröbisch et al., 2010). Based on the described
juvenile material of Stereosternum we can make two observations:
Ossification sequences. Generally in tetrapods, stylopod ossification starts before that of the
zeugopod and autopod, and mesopodial (wrist and ankle) ossification is
significantly delayed in relation to all other limb elements (Rieppel,
1993). In the articulated juvenile mesosaur, the mesopodial elements are not
yet ossified (Fig. 2b). In another isolated juvenile, attributed to
Stereosternum (NHMUK R3521), the astragalus is ossified but not the calcaneum. Therefore,
Stereosternum apparently follows the same ossification pattern in their mesopodia as the
sister-taxon Mesosaurus (Rieppel, 1993).
Growth rates. Mesosaurs display aquatic specializations in their limbs, with enlarged
zeugo- and autopodia in the hind limbs compared to those of the forelimbs
(Rossmann and Maisch, 1999). This size variation is also present in the
adult in MB.R.2089 (Fig. 1, Table 1).
First, taking the juvenile material into account, we calculated growth rates
for various limb elements in Stereosternum tumidum (Table 2). Results show that the hind limb
zeugopodia are more highly ossified, as demonstrated by the greater
longitudinal length of the elements (37.5 %) of the sub-adult as compared
to the humeri, femora, forelimb zeugopodia, and metatarsals (ranging from
26.5 to 35 %; Table 2). We associate this accelerated growth rate or
earlier onset of ossification to the more robust morphology of the adult
tibiae and fibulae (see epiphyseal widths in Table 1). This pattern is
potentially related to stronger hind limb bones needed for propulsion during
swimming. Such a phenomenon has been demonstrated for secondarily aquatic
skinks (Hugi et al., 2012). Microanatomical analyses would help shed light
on its internal strength parameters, such as bone density and cortical
thickness (Houssaye et al., 2016), but are not possible with the present
natural mold. Unfortunately, because no metacarpals are preserved, no
predictions can be made about such a pattern in the autopodia.
Secondly, in order to test for potential heterochronies, we established limb
growth ratios for another fossil reptile, Hovasaurus boulei from the Upper Permian of
Madagascar (Currie, 1981). Limb lengths and proportions in adult
Hovasaurus are in most respects very similar to those of Stereosternum (MB.R.2089). However; in
Hovasaurus, the hind limb zeugopod is not only substantially longer than that of the
forelimb in this taxon, it is also longer than the hindlimb zeugopod of
Stereosternum (Currie, 1981). In fact, growth rates of the humeri, femora, forelimb
zeugopodia, and metatarsals in Stereosternum and Hovasaurus are more or less similar (Table 2).
However, growth rates for the hind limb zeugopodia show a significant
difference: in Stereosternum the juvenile elements have already reached 37.5 % of the
adult length, in contrast to only 33.2–33.9 % in Hovasaurus (Table 2). This
accelerated growth rate or earlier onset of ossification in Stereosternum is surprising
given that hind limb zeugopodia in adult Hovasaurus are even longer than in adult
Stereosternum. Still, we suggest that this finding of skeletal heterochrony is related to
the aquatic lifestyle in Mesosauridae. In other extinct marine reptiles,
hyperdactyly and hyperphalangy were other adaptations to a fully aquatic
lifestyle (Caldwell, 2002). The relevant pattern in Hovasaurus remains to be
characterized.
Heterochronies (evolutionary shifts in developmental timing) are an
important tool for morphological change in the phenotype; e.g. limb
allometries result from differences in the growth patterns of skeletal
elements (Richardson, 1999). In Stereosternum, the advanced growth rate or earlier onset
of ossification in hind limb zeugopodia as compared to stylopodia and
forelimb zeugopodia, can be linked with longer zeugopodia and autopodia in
the adult and are secondarily related to a fully aquatic lifestyle (Rossmann
and Maisch, 1999). The autopodia in MB.R.2089 are not well preserved and
thus can not be evaluated here. This phenomenon, in which selection for an
adult trait produces crucial changes early in ontogeny, is called
developmental penetrance (Richardson, 1999). In fact, differences in the
phenotype are generated at a variety of ontogenetic stages (Richardson,
1999). Other mechanisms include changes at the cartilaginous level, e.g. in
fossorial talpid moles in which the cartilage anlage is already a miniature
of the adult phenotype including its distinct ecomorphological
specializations, as related to their extreme digging behaviour (Bickelmann
et al., 2014). Transcriptional heterochrony (changes in the spatial and
temporal expression of developmental genes during ontogeny) is another
developmental mechanism leading to morphological variation at the molecular
level (Richardson et al., 2009; Bickelmann et al., 2012). Here, only subtle
changes are needed to produce a significantly different phenotype
(Richardson, 1999). However, these are difficult, if not impossible, to
trace in the fossil record.
Our study shows evidence that differential growth rates and skeletal
heterochrony are developmental trajectories that could potentially account
for phenotypic variation in adult limb morphology, in this case related to
adaptation to a fully aquatic lifestyle in an extinct tetrapod clade as
early as 290 mya.
MBMuseum für Naturkunde Berlin, GermanyMNHNMuséum National d'Histoire Naturelle, Paris, FranceNHMUKNatural History Museum, London, UKSAMSouth African Museum, Cape Town, South Africa
CB and LAT contributed equally to the study design,
data analysis, and writing of the manuscript.
The authors declare that they have no conflict of
interest.
Acknowledgements
We thank Henrik Stöhr (Tübingen) for the
preparation of the latex cast. Carola Radke (Berlin) is thanked for taking
the photographs. Thanks to Oliver Hampe (Berlin) for access to the
collection under his care. We acknowledge constructive criticism by two
anonymous reviewers and the editor, which improved an earlier version of the
manuscript. This work was funded by the German Research Foundation (DFG), BI 1750/3-1 for Constanze Bickelmann.
Edited by: Johannes Müller
Reviewed by: two anonymous referees
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