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Home , Adinotherium, Archaeohyrax, Astrapotheria, Hegetotheriidae, Hegetotherium, Homalodotherium

INSTITUTIONEN FÖR BIOLOGI OCH MILJÖVETENSKAP

BODYMASS EVOLUTION IN SOUTH AMERICAN NATIVE (, MAMMALIA)

Atlanta Alexandra Koraszewicz

Uppsats för avläggande av naturvetenskaplig kandidatexamen med huvudområdet biologi BIO602 Biologi: Examensarbete 30 hp Grundnivå Termin/år: Vt 2019 Handledare: Juan David Carrillo, Gothenburg Global Biodiversity Center Examinator: Urban Olsson, Göteborgs Universitet 2 Illustration of an early notoungulate (Thomashuxleya externa) from the of Argentinian. Artwork by Stejpan Lukac (Carrillo and Asher 2017). Index

Abstract...... 2 Introduction...... 3 Material och methods...... 4 Abbreviations...... 4 Body mass data and age ranges of notoungulates...... 4 Phylogenetic analysis...... 4 Body mass evolution analysis...... 5 Results...... 5 Phylogenetic analysis...... 5 Body mass evolution in Notoungulata...... 8 Discussion...... 11 Limitations of the study...... 12 Conclusions...... 13 Acknowledgements...... 13 References...... 13 Appendix 1 – Ages of occurrence for notoungulate taxa...... 18 Appendix 2 – List of body masses ranges in Notoungulata...... 19

1 Abstract Body mass is an important trait that correlates with several ecological, life history and physiological features of a . Furthermore, body mass can be inferred from the record and therefore it can provide unique data to study trait evolution in geologic time. In this study I analyzed the body mass evolution of an extinct group of endemic south american ungulates (Notoungulata) that inhabited the continent during the . Notoungulata shows a wide body mass range and includes two main clades: Toxodontia (characterized by large taxa) and (characterized by small taxa). I collected information about body mass and age ranges for 75 notoungulate taxa from the literature. I combined 6 published morphological matrices to obtain a time-calibrated phylogeny of Notoungulata. The obtained phylogeny supports an age of 53 Ma for the origin of Notoungulata, 46 Ma for the origin of Toxodontia and 51 Ma for the origin of Typotheria. I used a Bayesian approach to estimate the ancestral body mass of the two main clades within Notoungulata and analyse the pattern of body mass evolution. The results show a clear divergence of large and small body masses between Toxodontia and Typotheria and suggests that the two clades followed different evolutionary paths. Notoungulata shows a large body mass range since its early history, following the evolutionary pattern of an early burst. This result is in accordance with the strong mammalian diversification that followed the – Paleogene event.

Keywords: Notoungulata, body mass, trait evolution, phylogeny,

2 Introduction Body mass is an important variable that correlates with several ecological and life history traits: the species habitat choice, their life mode, territorial ranges, diet and social behavior (Damuth & Macfadden, 1990). In fact, according to Damuth & Macfadden (1990) it may be one of the most important predictors of a species adaption to its environment. Body mass is widely studied in paleobiology and the fossil record can provide unique data to study the trait evolution in geologic time. The focus of this study is the Notoungulata, which was an endemic clade of -grade placentals that existed in South America through much of the Cenozoic. Notoungulata displayed a high diversity and broad and morphological variation with an especially striking spectra of body masses. Notoungulates were one of the most successful and diverse clades during their time (Croft, 1999). Their remains can be found from the late and all the way to the early where they have even been found alongside human remains (Billet, 2011), though the majority of taxa probably became extinct by the end of the (Prevosti et al. 2018, Slater, 2013). Notoungulates evolved during a time when South America was cut off from the other continents for a period that lasted from early-middle Eocene to the (Simpson, 1980). Though the perspective of a complete and prolonged isolation is now considered inaccurate (Wilf et al. 2013), there is no doubt that the period was incredibly significant for the future development of biotic diversity in South America. It's flora and fauna evolved in relative isolation resulting in a rich and unique endemic life quite unlike anywhere else in the world. In the early Pliocene the establishment of the Isthmus bridge between North and South America finally created a stable link between the two continents, and with it The Great American Biotic Interchange began (Simpson, 1980). By this time the population of native ungulates, including the notoungulates, were already much reduced. The exact cause of extinction is still unclear, though possible causes lie in the climatic changes that occurred during this time and the consequential change in the environment, as well as increased competition from the arrival of alien species from (Simpson, 1980). Notoungulates are one of five SANUs (South American Native Ungulates), together with , , and (Welker et al. 2015). These are sometimes grouped together in the superorder (McKenna, 1975). The taxonomic placement and relationship between the SANUs still remain under some dispute. Recent studies (Welker et al. 2015, Carrillo et al. 2018) show that Notoungulata and Litopterna could share a common ancestor with Perissodactyla (one-toed ungulates), which would suggest litopterns as the SANU closest related to the notoungulates. Notoungulata does not include any extant species. Though the phylogenetic relationship within the Notoungulata itself is not fully resolved (Billet, 2011), the order is considered to be monophyletic, as supported by the specific and skull structures unique to these ; notably the crochet on the upper metaloph, and the ear anatomy (Croft ,1999). Two main clades are distinct within the Notoungulata: the Toxodontia and the Typotheria. With the addition of Henricosborniidae and Notostylopiidae forming separate family groups of the oldest and most primitive notoungulates (Croft, 1999). The striking feature of the two main clades are the differences in size and morphological aspects. The toxodontids, were generally large, with some taxa indeed reaching sizes close to or even above that of the modern , while typotherians often did not reach sizes larger than that of a and also often exhibited many of the morphological traits of lagomorphs and (Croft, 1999). It is the aim of this project to establish the body mass evolution of the notoungulates, and perhaps gain one more step in discovering the history of these elusive but intriguing South American taxa.

3 Material och methods Abbreviations South American Land Ages (SALMAs). Lower molar row length (LMRL). Markov Chain Monte Carlo (MCMC).

Body mass data and age ranges of notoungulates Body mass estimates of 75 notoungulates were compiled from primary literature sources, making use of the scientific databases such as Web of Knowledge and Google scholar. The estimations used were mainly from dental and cranial parts due to their predominant availability in the fossil record. Where there were choices between multiple estimates, LMRL were chosen above others on the basis of being the most reliable estimate of the dental variables. In those cases were a taxon is known also by its postcranial elements these were considered as the post crania could be a more reliable indicator of the body mass in particular for the smaller species were the standard error usually is more negligible. The body mass for the two Xotodon species: X. major and X. cristatus, was estimated from the LMRL and using the equation of Damuth (1990) for non-selenodonts ungulates. Measurements for the LMRL for each species were taken with ImageJ from photographs of the specimens, provided by Armella (2018) fig 5. The age range of each notoungulate taxon were compiled from the literature. Most of the time intervals correspond to the chronostratigraphic units of the South American Land Mammal Ages, (SALMAs). The chronology of the SALMAs follows Woodburne (2014), Woodburne et al. (2014), Tomassini (2013) and Carrillo et al. (2018). A complete list of body mass data and ages can be found in appendices 1 and 2.

Phylogenetic analysis In order to obtain a time-calibrated phylogeny of Notoungulata, 6 matrices with morphological characters were combined: Carillo and Asher (2017) for Notoungulata with 68 taxa and 146 characters, Carillo et al. (2018) for with 28 taxa and 59 characters, Cerdeno et al. (2012) for with 22 taxa and 39 characters, Seoane et al. (2017) for with 24 taxa and 39 characters, Vera (2015) for Notopithecines with 28 taxa and 86 characters, and Cerdeno and Vera (2015) for Leontiniidae with 23 taxa and 81 characters. The matrices were edited in Mesquite (Maddison and Maddison, 2018) and taxa without body mass estimates were deleted. If the matrix included a as terminal taxon, all species with body mass data that belong to that genus, were coded with the same character states. If the matrix contained only one species of a genus, any additional species with body mass data from the same genus were added with ? as character state and the genera were constrained as monophyletic (see below). But if we had body mass data for an entire genus but not separate species and the matrix did have defined species from that genus, then all of the species in the matrix were kept. The edited matrices were then merged in R. Bayesian Inference was done using the program MrBayes 3.2.6 (Huelsenbeck and Ronquist, 2001). Time- Evidence Dating divergence times of the phylogeny was estimated by incorporating the known age ranges for the notoungulate taxa included in the matrix containing homologous morphological characters as described in Zhang et al. 2015. A rooted, relaxed clock model was chosen for the analysis and with Phenacodus as the outgroup.

4 To account for incomplete morphological data for some taxa several constraints were set on the basis of their monophyly as suggested by previous studies. Both main clades Toxodontia and Typotheria were constrained on the basis of monophyly suggested by Billet (2011). Furthermore, family constraints were set on Leontiniidae as supported by Cerdeno and Vera (2015), Homalodotheriidae and Toxodontidae (Billet, 2011), Mesotheriidae (Seoane et al. 2017 and Cerdeno et al. 2012), Hegetotheriidae (Vera et al. 2015 and Seoane et al. 2017), (Billet, 2011). Finally, constraints were set on the genera Colpodon, , , Xotodon, Trachytherus, , Eutypotherium, Typotheriopsis, Pseudotypotherium, Hemihegetotherium, Prohegetotherium, Paedotherium, Tremacyllus, , , , and Archeohyrax.

Body mass evolution analysis A Bayesian algorithm (“fossilized” Brownian motion) was used to study the body mass evolution of Notoungulata, following the example described by Silvestro et al. (2018). The analysis was performed using the FossilBM program available at https://github.com/dsilvestro/fossilBM. To account for the uncertainty of the body mass estimates of the , the runif function in the program R was used to generate a random estimate from a normal distribution within the range of the body mass (estimate plus or minus the standard deviation) for each taxon. A file containing the body mass data and the taxa names was then used together with one random tree from the posterior distribution of trees obtained in the phylogenetic analysis in MrBayes. Mean ancestral body masses where estimated for the main clades Notoungulata, Toxodontia and Typotheria. The node for most recent common ancestor was found using the MRCA function in the program R and then the mean body mass for that node was estimated from the posterior distribution of body masses obtained in the result from the FossilBM analysis.

Results Phylogenetic analysis The phylogenetic tree from the MrBayes analysis can be seen in Figure 1(a-c). The tree is rooted and based on a 50% majority rule consensus. The Figures 1 (b-c) show a closeup of the phylogeny for the two clades Toxodontia and Typotheria with the posterior probabilities of the nodes. The basal notoungulate taxon murinus is here placed as a sister taxon to the clade Toxodontia (Fig.1). Branch probability of 1, corresponds to a 100% probability, here showing where the branches where constrained. The posterior probability of the remaining nodes ranges from 0.5 to 0.9. The support for some nodes is low. The lower probabilities within Typotheria are notable for the nodes of Interatheriidae (0.58), the node diverging Prohegetotherium from and Hemihegetotherium (0.65), and the nodes linking the genera Eutypotherium with the rest of Mesotheriidae (0.63) as well as the node diverging Typotheriopsis within the same family (0.59). Within Toxodontia lower probability is shown for the node diverging the clades Leontiniidae with Toxodontiidae and part of Notohippiidae (0.67). Polytomies are visible within Toxodontia and Typotheria. Notably the nonmonophyletic families of (Fig. 1b), containing the genera Pleurostylodon, Thomashuxleya and Periphragnis and (Fig. 1c) with the genera Colbertia, Oldfieldthomasia, and Ultrapithecus as well as the family Acropitheciidae with Acropithecus. From the monophyletic

5 families the genera Antepithecus and Notopithecus from Interaheriidae, Typotheria, show polytomies. Figure 2. shows the estimated time of appearance for the clades of Notoungulata. Polytomic taxa lack data.

Figure 1. a-c Majority consensus tree generated in the program MrBayes for the order Notoungulata with closeups of the two main clades Toxodontia and Typotheria a) Cladogram showing all the notoungulate taxa used in this study with the mean divergence times for each node. Red highlight marks the clade Toxodontia, green highlight marks the clade Typotheria. b-c) Close up of cladograms for the clades Toxodontia and Typotheria. Numbers show the posterior probability of the node positions. 1 = 100% posterior probability. Observe that a full posterior probability here reflects that these clades and taxa were constrained prior to the analysis. Red numbers signify lower posterior probability.

a) Cladogram for the order Notoungulata

6 b)

Cladogram for the clade Toxodontia.

c)

Cladogram for the clade Typotheria

7 Figure 2 Time-calibrated phylogeny showing the estimated time of appearance for Notoungulata clades. Numbers on bars estimate the posterior probability of the diverging branches. 1=100% posterior probability.

Body mass evolution in Notoungulata For the three clades Notoungulata, Typotheria and Toxodontia the estimated mean ancestral body mass, for the most recent common ancestor, was as follows: Notoungulata = 4.0 kg; Typotheria = 3.72 kg and Toxodontia = 21.3 kg Figure 4 shows the evolution of body mass range of the Notoungulata. Around 53 Ma the body mass range of notoungulates underwent a rapid expansion. The majority of taxa from Toxodontia falls in the range of medium-large body masses (50-4000 kg) and the typotherian taxa in the range of small- medium body masses (0-50 kg), with a dominating proportion below 10 kg. Thus, the body masses are sorted into two distinct groupings, with little overlap between the two clades. Both small and large sizes coexisted during most of the Cenozoic. There is some variation in the body mass data over time within the respective clades. The body mass range within Toxodontia grows rapidly from the point of divergence 53 Ma. The families Homalodotheriidae and Isotemnidae keep a linear increase in body mass, Asmodeus reaching a size of 1679 kg, at 27 Ma, while shows a body mass of 405 kg. The rest of the Toxodontids diverge from Homalodotheriidae and Isotemnidae at 45 Ma. The Leontiniids Scarittia and , diverge at 34 Ma and reach large body masses close to that of Asmodeus, while the rest of the Toxodontids remain in a range below 200 kg. The Rhychippus genus diverges at 29 Ma, with Rhynchippus pumilus reaching 24 kg. Toxodontidae diverges at 22 Ma

8 into two branches with the genera Nesodon and Adinotherium on one hand and the remaining Toxodontidae on the other. Nesodon and Adinotherium diverge by 18 Ma, Nesodon reaching a body mass between 300-500 kg, while Adinotherium shows a range of 67-80 kg. The rest of the Toxodontiidae taxa first show a decline in size with Proadinotherium at 39 kg and then, at 21 Ma, then the clade rapidly increases in size, finally approaching 4000 kg with . For reference of the time of divergence for the clades of Notoungulata see Figure 1a. The clade Typotheria shows less variation, with the exception of the family Mesotheriidae (Fig 5). The family Mesotheriidae diverges from the rest of the of the typotherians around 32 Ma (see Figure 6 (a-b)), with the early mesotheriid genera Trachytherus reaching a body mass close to 400 kg. At 29 Ma, the rest of the mesotheriids diverge from Trachytherus. A branch with the genus Altitypotherium further diverges at 22 Ma reaching 12 kg. The last significant divergence in Mesotheriidae occurs at 15 Ma with the genus Eutypotherium reaching 15-25 kg and the genera Typotheriopsis, Mesotherium and Pseudotypotherium in the range of 80-260 kg.

Figure 4. Phylogenetic tree showing the body mass evolution in Notoungulates. This figure shows a simplified version (lacking some taxa) of the results for visualizations sake.

9 Figure 6 a) Cladogram of Typotheria with the mean divergence times, highlighting the family Mesotheriidae.

Figure 6 b) Cladogram of Mesotheriidae with mean divergence times.

10 Discussion The pattern that we see in the analysis result for the body mass evolution of Notoungulata suggests an evolutionary pattern called an ”early burst”. Contrary to a linear evolutionary pattern, where one would expect a gradual development of size from small body masses to large ones, an early burst shows a rapid, overall spread of diversity within different size ranges (Slater, 2013). During the Mesozoic, before the era of the notoungulates, the mammal fauna was strictly dominated by smaller sizes. A change occurred following the Cretaceous - Paleogene (K-Pg) , ~ 66 mya, when there is evidence that body mass diversity among mammals suddenly increased (Slater, 2013). This phenomenon has been widely discussed and it has been suggested that certain environmental factors can limit the diversification and spread of a species, effectively diminishing their development (Grossnickle et al. 2016). After such a constraint is removed, rapid development should be able to occur. It is possible that the consequence of the disappearance of large predators such as the , following the K-Pg extinction event, allowed mammals the freedom needed to develop a wider range of sizes. It is therefore reasonable to assume that the same applies to the notoungulates. Indeed, we can see in the diagram that the very first notoungulates are in the small to middle range of body mass, the estimated body mass for the most recent common ancestor for Notoungulata being ~ 4 kg. But after 53 Ma a rapid increase in the body mass range (early burst) is evident. We may wonder why the diversification didn't occur earlier since the K-Pg extinction event happened almost 7 million before the origin of Notoungulata. It is quite probable that the underlying factor lies in the environmental conditions. During the late Paleocene - early Eocene, 59-50 mya, climatic conditions where very warm, a time known as the Paleocene-Eocene thermal maximum (PETM), which had a peak around 52-50 mya (Prevosti et al. 2018). This would roughly correlate with the expansion of the notoungulates and might suggest that the warm, tropical environmental conditions where especially beneficial for their development, possibly in relation to the flourishing rainforest vegetation of this time, which consisted of a rich flora of angiosperms, conifers and ferns (Woodburne et al. 2014, Wilf et al. 2013). It is clear from the analysis, as well as from previous studies on this matter, that the evolutionary history of notoungulates took two very different roads: that of Typotheria and Toxodontia. The distinct division of sizes within the two groups are very striking, especially since both types of notoungulates seem to have coexisted in the same environments during the same time, as is suggested by the analysis as well as the strata in which the fossils where found. It is especially noteworthy that the divergence of Toxodontia and Typotheria are not the only time in the history of Notoungulates where clade took a sudden evolutionary turn from small to large size. The example of the typotherian family Mesotheriidae is in fact very similar to that of the first divergence of the two main clades. We can see in Fig. 5 that the family Mesotheriidae left off from the rest of the typotherians around 32 mya and is in this analysis the only family of typotherians than reached a body mass larger than 50 kg. Why did the clades differ in the pathways of body mass evolution? It is possible that some environmental factors such as a brief geographic speciation, could have led to the separation of these clades. In the case of Mesotheriidae, the time of divergence is close to the beginning of the Andean orogeny, ~30 mya, (Prevosti et al. 2018). Such a geographic isolation and possibly a subsequent renewed contact could perhaps explain why some taxa such as Altitypotherium and Eutypotherium later diverge back to the smaller body masses as this renewed connection may have allowed the taxa to adapt back to the environments that benefited smaller size in the first place. Apart from Mesotheriidae, the body mass ranges for toxodontians and Typotherians do not seem to overlap, however there is some considerable fluctuations in size within the two clades themselves, and especially within Toxodontia. For example, in Homalodotheriidae, we see a

11 sudden drop in body mass between Asmodeus and Homalodotherium, around 27 mya, with a difference in size from 1676 kg to 407 kg respectively. 21 mya in the family Toxodontiidae the body mass starts to increase from Proadinotherium, with a body mass of 39.5 kg, to Mixotoxodon, 4055 kg. Such a large difference as that between Proadinotherium and Mixotoxodon would suggest that both species, though from the same family, probably had very different habitat and dietary requirements. We know that the Cenozoic was a time of major environmental upturns, and practically throughout the existence of the notoungulates South America underwent severe environmental changes (Prevosti et al. 2018). This included the above-mentioned orogeny of the Andes with high seismic and volcanic activity, as well as global climate cooling. After the extremely warm period during the Paleocene-Eocene, temperatures began to gradually fall, dropping drastically with the beginning of the , ~34 mya (Prevosti et al. 2018). In accordance with the cooling, a change in the vegetation occurred replacing the rich, humid forests that had prevailed before with more open and arid grasslands (Pascual, 2006). In view of this it is easier to see what external forces worked on the evolution of the inhabitants of South America, and it is easier to understand why such fluctuations in body mass might have occurred. It is an interesting point that during the coldest period, at the very end of the notoungulate era, ~4-5 mya, we find some of the very largest toxodonts, including Mixotoxodon, as well as some of the very smallest typotherians. It is possible that this has a link to the lower metabolism requirements that comes with large size (Savage et al. 2007), allowing the largest individuals to persist even during cooler conditions. In contrast, the very smallest typotherians might possibly have had the advantage of being small enough to seek adequate cover, while the middle-sized ungulates got the shortest straw by being too large to hide and having too small a ratio between bodymass/ bodysurface to generate the warmth required to survive in the open.

Limitations of the study It is also important to note that the fossils on which this study is based, do not represent the notoungulate fauna for the entire South America. As for most fossils from this continent the majority of finds comes from (Croft, 2012). Because of a long history of sedimentation and favorable soil and climate conditions (Wilf et al. 2013, Croft, 2012), this region has been well suited for the preservation and availability of fossils. The central and northern parts of South America remain less studied. Despite important advances on the systematics of notoungulates, when establishing the phylogeny for this study multiple constraints were needed. One reason is that relying on purely morphological characters give limited information to obtain a well-resolved phylogeny. This is partly due to the effect of converging evolution which means that morphological characters can be shared among unrelated species because they have been adapted to similar environments (Alcock, 2013). The second reason is because we combined multiple matrices each containing different morphological characters, which meant that the combined matrix consisted of several taxa with incomplete data. As only the taxa which share data for the same morphological characters can be compared to each other, this will inevitably result in a restriction in the resolution. Because the constraints used were chosen only for those families and taxa that have been shown to be monophyletic by previous phylogenetic analyses, they can be considered reliable. However, as the monophyly of some families such as Isotemnidae and Notohippiidae have never been tested and could consequently not be constrained, these retained polytomies in the phylogeny. In view of the constraints, we must accept that no new information beyond that of previous studies could be gained from the resulting phylogeny.

12 As this study focused on the taxa with body mass data, it includes less than half the known existing taxa from Notoungulata and two thirds of this taxa was represented by Typotherians.The patterns recovered here should be further tested with the inclusion of additional taxa, especially from Toxodontia. A further reflection on the possible caveats of the body mass data must be made as well. First of all, a large part of the data for the body masses were obtained from the same publication, namely that of Elissamburu 2012. This may be a negligible fact, but for the sake of diminishing the risk of error in the calculations a comparison of data from various sources would have been preferable.

Conclusions The results from this analysis gives us a first glimpse of the body mass evolution in notoungulates. We know that the evolution of body mass in Notoungulata rapidly diversified around 53 mya taking on the pattern of an early burst. The clades Toxodontia and Typotheria sort into two distinct body mass ranges; Toxodonts dominating the medium-large body mass range and Typotherians the small body masses. There is little overlap between the clades, with the exception of the Typotherian family Mesotheriidae that reached the size range close to that of the Toxodontids. A more complete set of taxa and a phylogeny based on both morphological and molecular data would be most interesting to see, as well as an indepth comparison of the changing trends in the environmental conditions and the patterns seen in the body mass evolution for each diverging clade. Right now, it is obvious that there is still much to learn about this unusual South American order of mammals.

Acknowledgements I would like to thank my supervisor Juan D. Carrillo for his help and guidance in this project, and for giving me the opportunity to work on a fascinating subject. I would also like to thank Lotta Kvarnemo for her unwavering support, positive attitude and dedication to helping students at all hours. Finally, I want to thank my Mum for always believing in me and that I could do this, and for standing by me through it all, you’re the reason I’ve made it this far. Thank you!

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17 Appendix 1 – Ages of occurrence for notoungulate taxa

18 Appendix 2 – List of body masses ranges in Notoungulata

19