Palaeontology Extreme growth plasticity in the royalsocietypublishing.org/journal/rsbl early branching sauropodomorph Massospondylus carinatus
Research Kimberley E. J. Chapelle1,2, Jennifer Botha3,4 and Jonah N. Choiniere1 1Evolutionary Studies Institute, and 2School of Geosciences, University of the Witwatersrand, Cite this article: Chapelle KEJ, Botha J, Johannesburg, 2050 South Africa Choiniere JN. 2021 Extreme growth plasticity 3Karoo Palaeontology Department, National Museum, Bloemfontein, 9300 South Africa in the early branching sauropodomorph 4Department of Zoology and Entomology, University of the Free State, Bloemfontein, 9300 South Africa Massospondylus carinatus. Biol. Lett. 17: KEJC, 0000-0002-9991-0439 20200843. https://doi.org/10.1098/rsbl.2020.0843 There is growing evidence of developmental plasticity in early branching dino- saurs and their outgroups. This is reflected in disparate patterns of morphological and histological change during ontogeny. In fossils, only the osteohistological assessment of annual lines of arrested growth (LAGs) can Received: 27 November 2020 reveal the pace of skeletal growth. Some later branching non-bird dinosaur species appear to have followed an asymptotic growth pattern, with declining Accepted: 21 April 2021 growth rates at increasing ontogenetic ages. By contrast, the early branching sauropodomorph Plateosaurus trossingensis appears to have had plastic growth, suggesting that this was the plesiomorphic condition for dinosaurs. The South African sauropodomorph Massospondylus carinatus is an ideal Subject Areas: taxon in which to test this because it is known from a comprehensive onto- developmental biology, evolution, genetic series, it has recently been stratigraphically and taxonomically revised, and it lived at a time of ecosystem upheaval following the end-Triassic palaeontology extinction. Here, we report on the results of a femoral osteohistological study of M. carinatus comprising 20 individuals ranging from embryo to skeletally Keywords: mature. We find major variability in the spacing of the LAGs and infer developmental plasticity, growth, disparate body masses for M. carinatus individuals at given ontogenetic osteohistology, basal sauropodomorph, ages, contradicting previous studies. These findings are consistent with a lines of arrested growth high degree of growth plasticity in M. carinatus.
Author for correspondence: Kimberley E. J. Chapelle 1. Introduction e-mail: [email protected] Osteohistological growth lines are widely used to infer dinosaurian growth tra- jectories [1]. Such growth lines are evidence that extinct dinosaurs exhibited growth rates exceeding those of living reptiles, and which were below, equal Downloaded from https://royalsocietypublishing.org/ on 12 May 2021 to, or exceeded those of extant birds and mammals depending on the lineage in question [2–4]. However, inferring dinosaur growth trajectories and curves using growth lines across large ontogenetic samples often invokes assumptions about asymptotic growth, which are not always in accord with osteohistological observations [1]. Organisms can alter their growth strategies in response to environmental cues, a process generally referred to as ‘developmental plasticity’ [5]. Two types of phenotypic developmental plasticity were originally defined: that in which organisms are genetically adapted to use the environment to trigger certain phenotypic changes (i.e. ‘developmental conversion’ in [5]) or that in which they passively respond to environmental variation (‘phenotypic modulation’ in [5]). Developmental plasticity involving phenotypic modulation (hereafter Electronic supplementary material is available simply ‘developmental plasticity’) has been reported in many living and extinct online at https://doi.org/10.6084/m9.figshare. tetrapods based on a variety of evidence, including: delays in maturation c.5416965. (e.g. the appearance of feathers or neurocentral fusion, see [6]), morphological
© 2021 The Author(s) Published by the Royal Society. All rights reserved. plasticity (e.g. changes in discrete characters, see [7]) and 2. Methods 2 osteohistological growth plasticity [8,9]. Osteohistological We combined historically produced [17] and newly made osteo- royalsocietypublishing.org/journal/rsbl growth plasticity (hereafter ‘growth plasticity’) is well known histological sections from the femora of 20 specimens from in living tetrapod taxa, including birds [6,10] and amphibians different upper Elliot Formation localities in South Africa that [11,12]. In these groups, it results from unfavourable conditions could be confidently referred to M. carinatus (table 1; electronic during organismal growth that reduce available energy necess- supplementary material, table S1). We made new osteohistologi- ary to deposit bone tissues, which in turn leads to decreases cal sections at the National Museum, Bloemfontein following in annual growth rates [6]. Such variation in annual growth standard methods recently described in the literature [41,42]. rates can cause deviations from the idealized asymptotic Complete sections were taken at the midshaft where possible growth trajectory thought to characterize many living and (see electronic supplementary material, S2–S4 for more details extinct tetrapod groups. on sections). We also added digital osteohistological data from Growth plasticity is the best metric for developmental plas- propagation phase-contrast synchrotron radiation micro-com- ticity in the fossil record because it provides correlated age and puted tomography scans of the embryonic specimen BP/1/ 5347a done at the European Synchrotron Radiation Facility (Gre- size data that can be used to assess annual gains in body mass. Lett. Biol. noble, France) with an isotropic voxel size of 13.11 µm. Growth plasticity is well studied in non-mammalian therap- – We counted double and triple lines of arrested growth sids [13] and in early branching amphibians [14 16], but has (LAGs) as a single unit if no vascularization was present between
been poorly explored in dinosaurs. Early osteohistological them. We measured osteohistological sections in ImageJ 1.52a 17 studies of dinosaurian growth in the early branching sauropo- [43] and generated figures both in RStudio v. 1.1.453 [44] using 20200843 : domorph (EBSM) Massospondylus carinatus suggested a close the ggplot 2 package [45] and Inkscape 1.0 [46]. Measurements correlation between age and size [17]. This hypothesis was con- were taken in the thickest part of the cortex and along a single tradicted by the first explicit studies of growth plasticity in radius extending from the middle of the sections to the sub-peri- early dinosaurs in 2005 by Sander & Klein [9], and later osteal surface (see electronic supplementary material, S4). Line expanded upon by Klein & Sander [8] in 2007, who studied drawing tracings of a representative sample of our thin sections the EBSM Plateosaurus trossingensis. Since then, only a handful were done to show the growth marks in their entirety (see elec- tronic supplementary material, figures S2 and S3). This work of studies have investigated any form of developmental was approved for destructive sampling by the South African plasticity in dinosaurs [18], and these have largely focused Heritage Resources Agency (permit no. 2643), and additional on external markers of plasticity such as muscle insertion methodological descriptions are provided in electronic sup- scars [19]. plementary material, S4. Understanding growth plasticity is important for eluci- dating growth rates, sexual maturation timing, metabolism and taphonomic profiling of populations [1,4,9,20–22]. This is in turn useful for understanding how palaeoecosystems 3. Results developed and the mechanisms responsible for population The embryonic specimen (n = 1) has a femoral circumference and taxonomic diversities [14]. Ascertaining growth plasticity (FC) of 4.90 mm (estimated body mass of 0.017 kg, 2.29% of in dinosaurs is therefore an area where there is great poten- the largest specimen, i.e. the neotype BP/1/4934) whereas tial for palaeobiological advances, but one that is hindered the post-hatching specimens (n = 19) range in size from an FC by the rarity of fossil sample sets spanning the full ontogen- of 50.50 mm (10.183 kg, 23.60% of the largest specimen) to an etic sequence of a single taxon. EBSMs present potential FC of 214 mm (543.200 kg, represented by the largest speci- solutions to these limiting factors, as several genera are men) (table 1). There is only one specimen with a femoral known from large sample sizes containing multiple growth circumference larger than 160 mm (i.e. 75% of the largest speci- stages [9,22–29]. men). This is in agreement with Myhrvold [47], who indicated The basal sauropodomorph dinosaur M. carinatus is the that mature (fully or nearly grown) individuals are underrepre- most abundant dinosaur fossil found in southern Africa, sented in a wide variety of dinosaur groups. with hundreds of specimens ranging in size from embryos Cyclically deposited fibrolamellar bone is the predominant to inferred skeletally mature individuals [28,30–32]. Massos- bone tissue pattern during early and mid-ontogeny. Our sec- pondylus carinatus fossils are found in the upper Elliot and tions show a transition to slower forming parallel-fibred Downloaded from https://royalsocietypublishing.org/ on 12 May 2021 Clarens formations of the Stormberg Group in South Africa bone during very late ontogeny. The bone tissue is interrupted and Lesotho as well as correlated strata in Zimbabwe [32– by irregularly spaced LAGs indicating temporary cessations in 35]. These units are generally considered to be Lower growth (see electronic supplementary material, figures S2, S3 Jurassic in age and record the period immediately following and S5–S7 for sections). Dense secondary remodelling only the end-Triassic extinction event [36–39]. appears in the inner- to mid-cortex of the largest specimen, Its early branching phylogenetic position, high abundance, BP/1/4934. Although this specimen does not have an external recently revised taxonomic identification and stratigraphic fundamental system, several features suggest that this speci- position make M. carinatus an ideal taxon for studying men was an adult when it died (see [32]). dinosaur growth strategies and for testing if the plasticity The spacing between LAGs, the number of LAGs and the observed in P. trossingensis is a more broadly distributed sizes of the femora are highly variable among the specimens feature of EBSMs. Chinsamy’s [17] pioneering study of we sampled (summarized in figure 1 and table 1; see elec- M. carinatus femora was the first comprehensive work done tronic supplementary material, figures S2, S3 and S5–S7). on basal sauropodomorph bone histology. The advances in Only four specimens show a pattern of incrementally osteohistology in the past three decades make it an opportune decreasing LAG spacing towards the outer cortex, as is time to reconsider previous data and to bring abundant new hypothesized for asymptotic growth. The embryo and smal- data to bear on the question of the life-history and growth lest post-hatching specimen do not preserve any LAGs. The trajectory of M. carinatus. second smallest post-hatching specimen (35.05% of the Table 1. Specimens sectioned for the analysis, with their absolute size (based on the minimum circumference of the femoral shaft), their relative size (based 3 on the minimum circumference of the femoral shaft) compared with the largest specimen in the analysis, their inferred body mass (using the methods for royalsocietypublishing.org/journal/rsbl bipeds proposed by [40]), the number of observed LAGs, and notes on the presence of multiple LAG occurrences. Asterisks (*) indicate specimens for which slides were available from [17].
specimen femoral % largest body no. observed LAG number circumference (mm) specimen size mass (kg) LAGs pattern
BP/1/5347a 4.90 2.29 0.017 0 no LAGs BP/1/5253* 50.50 23.60 10.183 0 no LAGs BP/1/4266b* 75 35.05 30.263 5 single BP/1/5238 81 37.85 37.408 5 single
BP/1/5143* 83 38.79 40.007 8 single, double, triple Lett. Biol. BP/1/4267 85 39.72 42.719 5 single, double BP/1/4751 93 43.46 54.727 5 single 17
BP/1/4747* 95 44.39 58.030 4 single 20200843 : BP/1/5193 100 46.73 66.834 6 single BP/1/5397 100 46.73 66.834 5 single BP/1/4777* 105.75 49.42 77.960 8 single, triple BP/1/4693* 112 52.34 91.316 8 single NMQR3055 114 53.27 95.877 6 single BP/1/4860 143 66.82 178.976 4 single BP/1/5241* 145 67.76 185.955 9 single, double BP/1/4998 145 67.76 185.955 4 single BP/1/5108 145 67.76 185.955 9 single, double BP/1/4861* 159 74.30 239.689 9 single BP/1/4928 160 74.77 243.863 7 single BP/1/4934 214 100 543.200 7 single, double
largest specimen size) preserves five LAGs. The three speci- expansion cannot explain the high variance in LAG spacing mens with the most LAGs preserved (nine LAGs) range in between specimens or the differing number of LAGs in size from 67.76 to 74.30% of the largest specimen size. The femora of specimens of the same size (based on minimal largest specimen (BP/1/4934) preserves seven LAGs. Four femoral circumference). The latter could occur if the medul- specimens (BP/1/4860, BP/1/5241, BP/1/4998 and BP/1/ lary cavity itself was variable in size. M. carinatus displays 5108) of similar sizes (between 66.82 and 67.76% of the largest no consistent trends in LAG spacing at any size or histologi- specimen size) preserve different numbers of LAGs with cal age (figure 1), a pattern similar to observations in the varying spacing between them. Six specimens display EBSM P. trossingensis [8] (see electronic supplementary double and triple LAGs. These double and triple LAGs are material, S4 for further discussion), but markedly contrasting sporadically distributed in the cortex with no generalizable with the more channelized late branching dinosaurs which pattern except for BP/1/4934, which only has double LAGs show decreasing inter-LAG spacing over time (reflecting in the outer cortex (table 1; electronic supplementary slowing growth towards adulthood) [1,51], Interestingly, a Downloaded from https://royalsocietypublishing.org/ on 12 May 2021 material, figures S5–S7). subset of the larger M. carinatus specimens clearly retained the ability to grow rapidly into late ontogeny, occasionally growing faster, i.e., showing a wider distance between LAGs than some of the smaller individuals (e.g. the distance 4. Discussion between LAGs 6 and 7 in BP/1/5241 is larger than most of The specimens of M. carinatus sampled here are extremely the LAG spacings in the smaller individuals). Inter-LAG spa- variable in the relationship between body size and number cing differences, as measured here, can reflect profound of LAGs preserved (table 1), in their distribution of single, differences in annual body mass gain because of the scaling double and triple LAGs (table 1), and in the spacing between relationship with femoral circumference—a linear increase LAGs (figure 1). Although some LAGs in the inner-cortex in LAG spacing equates to a cubic increase in predicted may have been destroyed through resorption and remodel- body mass [40]. ling [48–50], secondary remodelling is only extensive in the In order to account for missing LAGs (through remodelling largest specimen (BP/1/4934; electronic supplementary or medullary cavity expansions), it is common to estimate the material, figure S7). Medullary cavity expansion can destroy actual ages of specimens by superimposing a size series of LAGs and be responsible for the differing number of LAGs cross-sections [48]. This has been used to study growth series in different elements, leading to intraskeletal variation in dinosaurs, such as in Chinsamy’s [17] study of M. carinatus within a specimen [48]. However, medullary cavity femora. Another method used for retrocalculating missing 4
20 000 200 royalsocietypublishing.org/journal/rsbl
17 500 175
15 000 150 m) 12 500 125
10 000 100 il Lett. Biol. LAG distance ( LAG circumference (mm) 7500 75 17
5000 50 20200843 :
2500 25
0 0
BP/1/5347BP/1/5253BP/1/4266BP/1/5238BP/1/5143BP/1/4267BP/1/4751BP/1/4747BP/1/5193BP/1/5397BP/1/4777BP/1/4693 BP/1/4860BP/1/5241BP/1/4998BP/1/5108BP/1/4861BP/1/4928BP/1/4934 NMQR3055 Figure 1. Spacing (in µm) between the femoral medullary cavity margin, LAGs and the sub-periosteal surface. The first, purple bar represents the distance from the medullary cavity (0 on the y-axis) to the first LAG, which can be affected by resorption and remodelling. The last bar represents the distance between the last recorded LAG and the sub-periosteal margin, which records the last and possibly incomplete interval of growth for the specimen. Other bar colours represent the inter-LAG distances between the first and nth LAG. Specimens are arranged left to right from smallest to largest based on femoral circumference represented by the red dotted line. Specimens in blue type have osteohistological section line drawings provided in electronic supplementary material, figures S2 and S3.
LAGs is the division of the inner part of a given section by the the fossil record. Some Triassic therapsid lineages that survived width of the minimum/maximum growth cycle (i.e. spacing the end-Permian extinction have been found to differ from between two LAGs) [4,8,9]. The weak relationship between Permian therapsids in that they are reproductively mature at age and body size that we find here shows that both of these smaller body sizes [20]. This entails that the maturation rates methods are particularly inaccurate for M. carinatus and of these individuals surpassed their growth rates, leading to likely for EBSMs because of the similar condition observed in stunted mature individuals, which points to imposed develop- P. trossingensis [9]. mental plasticity. Similarly, the high amount of morphological The high variance in LAG number and spacing through- developmental plasticity observed in some dinosaurs suggests out the sample makes traditional sigmoidal growth curves decoupling of the maturity and growth rate, indicating and inflection-based estimates of sexual maturation extre- imposed developmental plasticity [19]. mely inaccurate for M. carinatus, a caution to be observed High-amplitude fluctuations in climatic conditions [52] are in addition to concerns about sample sizes and statistical hypothesized to have excluded early dinosaurs from low- model selection [47]. Furthermore, the variability in LAG palaeolatitude communities throughout the Late Triassic Downloaded from https://royalsocietypublishing.org/ on 12 May 2021 numbers in similarly sized specimens makes predictions of by confounding their rapid growth (potentially enabled by age based on size (e.g. length or circumference of long elevated metabolisms [9]). The presence of extreme growth bones) inaccurate (contra [17]). This has far-ranging impli- plasticity in the Late Triassic basal sauropodomorph cations for taphonomy, e.g. population age profiles for P. trossingensis and the Early Jurassic basal sauropodomorph early branching dinosaur lineages based on size could be M. carinatus suggests that at least EBSMs retained the ability confounded by growth plasticity. to respond (via changing skeletal growth) to climatic and Studies of living taxa differentiate between induced and resource fluctuations throughout the Triassic–Jurassic tran- imposed developmental plasticity when body size growth is sition, and that environments at higher latitudes were also slowed owing to lack of resources [6]. In an induced plasticity relatively unstable during that time period. More generally, scenario, individuals slow their tissue maturation rate in developmental plasticity (morphological or growth) appears accordance with their decreased growth rate, whereas in an to have been common in early dinosaurs [18,19]. It provides imposed scenario, tissue maturation continues at the normal a potential preadaptive feature of dinosaurs that allowed rate. In the imposed scenario, the growth rate may either them to thrive in unstable post-extinction environments. accelerate once conditions are better (leading to a normal Comparative observations of developmental plasticity body size at maturity) or fail to catch up to tissue maturity (morphological or growth) in the fossil record are sparse and (leading to a stunted body size in a mature individual) [6]. span a large phylogenetic, temporal and geographic range, Differentiating between these two scenarios is challenging in making testing the link between environment and growth difficult in deep time [14,19,53]. A major outstanding question indicates that it may reflect a plesiomorphic feature in tetra- 5 is how broadly morphological developmental plasticity is pods and in that context is potentially a preadaptation that royalsocietypublishing.org/journal/rsbl reflected in the bone histology and how persistent develop- allowed early dinosaurs to thrive after the end-Triassic extinc- mental plasticity is within tetrapod lineages. A recent study tion. The extreme variability of M. carinatus suggests caution finds growth plasticity even in extant lineages—for example, should be taken when predicting ages and studying certain the rate of bone formation in modern quail responds to vari- aspects of physiology such as the timing of sexual maturity ation in environmental conditions [10]. These lines of in early branching dinosaurs. evidence point to growth plasticity being plesiomorphic for tetrapods in general or widely spread via convergence. Ethics. This work was approved for destructive sampling by the South In later branching lineages, where growth is generally con- African Heritage Resources Agency (permit no. 2643). sidered to be more channelized (e.g. Cretaceous dinosaurs Data accessibility. All data files are presented in the electronic and mammals), such plasticity has perhaps been overprinted supplementary material. by the evolution of derived metabolic pathways [9], which Authors’ contributions. K.E.J.C carried out the osteohistology laboratory
may provide a buffer to environmental fluctuations, either work, analysed the data, participated in the design of the study Lett. Biol. by increasing the ability to gather resources or by allowing and led the writing of the manuscript; J.B. assisted with data analysis, more rapid growth once conditions become more optimal. participated in the design of the study and edited the manuscript; J.N.C. participated in the design of the study, assisted with data More data on the distribution of growth plasticity in extinct analysis and edited the manuscript. All authors gave final approval 17 taxa and higher resolution Mesozoic climatic reconstructions for publication and agree to be held accountable for the work 20200843 : will help address this shortcoming. performed herein. Competing interests. We declare we have no competing interests. Funding. This study was funded by DSI-NRF Centre of Excellence in Palaeosciences (CoE-Pal) (to K.E.J.C., J.B. and J.N.C.), National 5. Conclusion Research Foundation South Africa (UID 117704 to J.B., UID 98800 and UID 118794 to J.N.C.) and the Palaeontological Scientific Trust The EBSM dinosaur M. carinatus is an ideal study taxon for (PAST) (to K.E.J.C. and J.B.). investigating intraspecific developmental plasticity in dino- Acknowledgements. Sifelani Jirah and Elize Butler facilitated collections saurs. M. carinatus had high intraspecific variability in LAG access. Bernhard Zipfel assisted with osteohistological sampling per- counts, LAG spacing and LAG patterns, indicating extreme mits. Sekhomotso Gubuza provided exceptional help creating and growth plasticity. Induced or imposed growth plasticity in cataloguing the osteohistological sections. Vincent Fernandez and M. carinatus may have been exacerbated by unstable environ- Paul Tafforeau supervised and conducted scanning at the European Synchrotron Radiation Facility. Martin Sander and Sterling Nesbitt ments in the Early Jurassic in the immediate wake of the end- offered useful discussion during the project. Martin Sander and Triassic extinction. The wide phylogenetic, spatial and tem- three anonymous referees are thanked for their helpful comments poral range of taxa displaying developmental plasticity during the reviewing process.
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