sign in sign up
<<
Home , Adinotherium, Archaeohyracidae, Hegetotheriidae, Interatheriidae, Mesotheriidae, Mesotherium

Ontogenetic and life history trait changes associated with convergent ecological specializations in extinct

Helder Gomes Rodriguesa,b,1, Anthony Herrelb, and Guillaume Billeta

aSorbonne Universités, Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements, UMR CNRS 7207, CP 38, Muséum National d’Histoire Naturelle, 75005 Paris, France; and bMécanismes Adaptatifs et Evolution, UMR CNRS 7179, Bâtiment Anatomie Comparée, CP 55, Muséum National d’Histoire Naturelle, 75005 Paris, France

Edited by Mikael Fortelius, University of Helsinki, Helsinki, Finland, and accepted by Editorial Board Member David Jablonski December 15, 2016 (received for review August 22, 2016) Investigating life history traits in mammals is crucial to understand (e.g., humans, hippos, rhinos) (11). However, this relationship, their survival in changing environments. However, these param- previously summarized under Schultz’s “rule,” cannot be general- eters are hard to estimate in a macroevolutionary context. Here ized to all mammals (12, 13). It has also been suggested that the we show that the use of dental ontogenetic parameters can provide time of eruption of the first molars is a suitable predictor of the pace clues to better understand the adaptive nature of phenotypic traits of life (e.g., longevity, maturity, weaning period) in some mammals in extinct such as South American notoungulates. This (e.g., primates, ruminants) (10, 12). Consequently, the scrutiny of recently extinct order of mammals evolved in a context of important dental ontogenetic patterns may prove very insightful to understand geological, climatic, and environmental variations. Interestingly, changes in life history and ecology, and therefore to assess the notoungulates were mostly herbivorous and acquired high- impact of environmental changes on extinct mammals. crowned teeth very early in their evolutionary history. We focused During the , the long isolated South American conti- on the variations in crown height, dental eruption pattern, and nent underwent drastic geological, climatic, and environmental associated body mass of 69 notoungulate taxa, placed in their changes that might have severely affected endemic mammalian phylogenetic and geological contexts. We showed that notoungu- faunas (14–17). Among these mammals, the extinct order of lates evolved higher crowns several times between 45 and 20 Ma, was highly diversified taxonomically and consisted of independently of the variation in body mass. Interestingly, the -sized up to rhino-sized taxa (18–20). They exhibited very independent acquisitions of ever-growing teeth were systemati- advanced dental specializations thought to be related to herbivory cally accompanied by eruption of molars faster than permanent (21, 22). Interestingly, high-crowned teeth (i.e., hypsodonty) evolved premolars. These repeated associations of dental innovations have among notoungulates during the Paleogene more than 10 million never been documented for other mammals and raise questions on years before their appearance in the majority of other mammalian their significance and causal relationships. We suggest that these groups (17, 21–24). For instance, intense crown height increase correlated changes could originate from ontogenetic adjustments occurred during the Middle – period in mammals favored by structural constraints, and may indicate accelerated life from northern continents, such as ruminants, and also perissodactyls histories. Complementarily, these more durable and efficient (e.g., Equidae, Elasmotheriinae) (8, 21, 22, 24), the closest extant dentitions could be selected to cope with important ingestions of relatives of notoungulates (25, 26). Most remarkably, a crown height abrasive particles in the context of intensified volcanism and increase convergently evolved in four distinct notoungulate clades increasing aridity. This study demonstrates that assessing both life history and ecological traits allows a better knowledge of the Significance specializations of extinct mammals that evolved under strong environmental constraints. Estimating life history traits such as pace of growth or lon- gevity is difficult in extinct mammals. Yet, these parameters dental ontogeny | hypsodonty | abrasion | notoungulates | could be helpful to better understand how herbivorous mam- mals adapted to changing environments. We here highlight the n understanding of the life history of mammals in their insights gained by studying dental growth and eruption in a Aecological context is essential to predict how these clade of extinct ungulate mammals. Variation in these traits may have coped with past environmental and climatic variations. was assessed in the context of volcanism, cooling, and in- The life history of mammals reflects behavioral, physiological, and creasing aridity in South America starting 50 Ma. We show that anatomical adaptations that have a direct impact on survival and ever-growing teeth combined with faster eruption arose reproductive success (1). Life history traits are in turn directly several times during the evolution of these mammals, allowing influenced by size and lifestyle, reflecting the adaptations of mam- them to obtain a more durable and efficient dentition in con- mals to their environment (2, 3). However, life history parameters straining environments. These innovations might represent such as fecundity, the age at sexual maturity, longevity, or mortality convergent ontogenetic and physiological adjustments that often cannot be quantified precisely in extinct species. Estimations of contributed to their ecological specialization. body size (or mass) alone do not allow accurate inferences on life history traits because of intrinsic variations depending on ecological Author contributions: H.G.R., A.H., and G.B. designed research; H.G.R. and G.B. performed factors (2, 4). For these reasons, bone histology is frequently used in research; H.G.R. and G.B. contributed new reagents/analytic tools; H.G.R. and G.B. ana- lyzed data; and H.G.R., A.H., and G.B. wrote the paper. extinct species for physiological inferences (5, 6). The authors declare no conflict of interest. Dental growth measured using crown height can, however, pro- – This article is a PNAS Direct Submission. M.F. is a Guest Editor invited by the Editorial vide data on both ecology and longevity (7 9). Moreover, studying Board. dental replacement, especially the timing of postcanine eruption, 1To whom correspondence should be addressed. Email: helder.gomes-rodrigues@ can give insights into the pace of life or ecology (10–12). The late mnhn.fr. EVOLUTION eruption of molars compared with permanent premolars can for This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. instance be associated with a slow pace of growth in some mammals 1073/pnas.1614029114/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1614029114 PNAS | January 31, 2017 | vol. 114 | no. 5 | 1069–1074 Downloaded by guest on September 27, 2021 (e.g., , , , and Hegeto- Interatheriidae, whereas they have similar variations regarding theriidae). This repeated innovation was likely selected to withstand crown height. As a result, it can be considered that a crown high dental wear during mastication (17, 27). It was also assumed to height increase is not directly influenced by body mass, as was be related to the successive orogenic, volcanic, and erosive phases of previously suggested for some notoungulates (31) and other the Andean Cordillera starting from the Late (approxi- mammals (9). mately 57 Ma) (28), which involved subsequent deposition of Because they lived in environments on which soil minerals abrasive detritic particles on plants (16, 29, 30). (dust and grit) were likely deposited to an important degree due The comparative ecology and life history of the different to volcanic activity (16, 17, 29), high-crowned teeth may have groups of notoungulates remains, however, poorly understood. allowed notoungulates to cope with the ingestion of such exter- Here, we provide data allowing a more complete overview of the nal abrasive particles that strongly wear teeth during chewing. In convergent crown height increases and associated dental onto- the presence of external abrasives, wear rates may have also been genetic changes in notoungulates to better understand their enhanced by an increase in the pressure and intensity of chewing, evolution with respect to environmental variations taking place especially given a diet including many fibrous plants with a low in South America from the Late Paleocene onwards. For this nutritive value (e.g., grass and grass-like plants, some shrubs) reason, we studied and compared the evolutionary patterns of (27). This increase might also be related with digestive abilities dental growth (Fig. 1A) and eruption (Fig. 1B) in different clades assumedtobelessefficientinnotoungulatesthanruminants, of notoungulates along with estimated body mass in the context but closer to those of their extant relatives (e.g., horses, rhinos), of a consensual and well-resolved phylogeny. We also put these for which the amount of food intake is higher and the chewing original data into a geological framework to estimate the varia- effort greater (17). It is important to point out that the pres- tions in ecological and life history traits that may be related to ence of abundant external abrasive particles would have espe- major geological and climatic events during that time. cially affected animals eating a greater proportion of plants close to the soil (i.e., herbaceous to shrubby plants). That may Results and Discussion have been the case of some South American mammals, such Convergent Increase of Dental Crown Height in Notoungulates. The as notoungulates, small argylagoid marsupials, and ground- parsimony reconstruction of character evolution indicates that dwelling caviomorph , which convergently acquired notoungulates acquired high-crowned cheek teeth at least three high-crowned dentitions (17). times during their evolutionary history (Fig. 2). Specialization toward ever-growing dentitions (i.e., hypselodonty) then con- Striking Convergent Modifications of Dental Eruption Patterns and vergently spread among the four last-existing monophyletic Life History Traits. Data on the modes of dental eruption show a families of notoungulates (Toxodontidae, Interatheriidae, Mes- very similar distribution to crown height on the cladogram, with a otheriidae, and ). As is evident from the exam- reversal from third molars erupting last to third molars erupting ination of phylogenetic distributions (Fig. 2), there is no faster than permanent premolars in the four late diverging significant correlation between crown height and estimated body families (Fig. 2). The details of their eruption sequence slightly mass in notoungulates. Such a lack of a significant correlation is differ from one clade to another (Fig. 2). Indeed, in Tox- exemplified by the Toxodontidae, and most of Mesotheriidae, odontidae, the eruption of third molars occurs only before the which show larger body masses than the Hegetotheriidae and eruption of the last permanent premolars (P4), as observed in

Fig. 1. Main variations of dental growth and eruption observed in notoungulates. (A) Dental crown height states (Colbertia magellanica AMNH49873, Pseudhyrax sp. MLP61-IV-9–1, Paedotherium bonaerense MNHN.F.MHR45). (B) Dental eruption states (Trachytherus alloxus MNHN-BOL-V 009027, Micro- typotherium choquecotense MNHN-BOL-V 003349). P, premolars; M, molars.

1070 | www.pnas.org/cgi/doi/10.1073/pnas.1614029114 Gomes Rodrigues et al. Downloaded by guest on September 27, 2021 Fig. 2. Comparison of the distributions of crown height states, body mass, and modes of dental eruption on the composite tree of notoungulates (Material and Methods provide details). Red branches emphasize the repeated codistributions of ever-growing cheek teeth and faster eruption of molars in the highlighted clades of notoungulates. Gray and orange branches represent the other states for each character depicted in the captions. Black branches represent an absence of data for the respective character. P, premolars; M, molars. Names of Plesiotypotherium achirense, “Plesiotypotherium” minus, Trachytherus spegazzinianus, and Trachytherus alloxus were shortened. *Taxa for which timing of dental eruption relative to skull growth is known and discussed in the text (33, 34).

horses (11). In contrast, the third molar erupts before the there is only a slight discrepancy in dental eruption between eruption of most permanent premolars (P2–P4) in these taxa (Fig. 2). In and , the molars (i.e., the Hegetotheriidae, Interatheriidae, and Mesotheriidae), a were all erupted at 100% and 85% of the adult skull size, re- pattern known in many specialized , including rumi- spectively (33). In addition, the first molars also erupted earlier nants (11). in Nesodon (60% of the adult skull size) than in Adinotherium Interestingly, it has been proposed that both horses and ru- (70% of the adult skull size). Thus, both the faster eruption of minants show a relative fast pace of growth (2) associated with molars compared with permanent premolars, and precocious faster molar eruption (11). A faster eruption of the third molars eruption of first molars compared with skull growth may suggest compared with permanent premolars was first observed in a a faster life history in some late diverging clades of notoungu- mesotheriid by Townsend and Croft (32), who proposed a faster lates (Fig. 2), especially compared with similar trends observed growth for this notoungulate, although they acknowledged not in extant ruminants, horses, and some primates (10–12). having enough data to further substantiate their observations. It is worth mentioning that body size (or body mass) is known More recently, a few craniodental ontogenetic series were de- to constrain life history evolution in mammals to a large degree scribed in Mesotheriidae and Toxodontidae (33), which enabled (2, 4, 12). In that context, the interpretation of the sequence and study of genera showing skulls at different states of dental eruption (Fig. 2, Trachytherus and ; Adinotherium timing of dental eruption into pace of growth patterns should be and Nesodon). Interestingly, the entire set of molars erupted considered with caution. However, body mass appears to play a much faster compared with cranial growth in the late diverging reduced role regarding ontogenetic dental changes in notoun- mesotheriid , Mesotherium, than in the earliest known ge- gulates (Fig. 2). Moreover, in specialized taxa, such as herbi- nus, Trachytherus. More precisely, the eruption of all of the vores, and in unstable environments, life history traits were molars was completed in specimens of Mesotherium presenting a shown to be more dependent on ecology than on body size (2, 4). skull that was only 50–60% of the adult skull size (34). In con- This may also hold true for notoungulates. In addition to these trast, the first molars were not yet erupted at this stage in Tra- putative changes in life history, the repeated acquisition of a chytherus, and the eruption of all molars was completed only in faster molar eruption in notoungulates can also be related to a adults (33). In toxodontids, the comparison of Adinotherium and faster acquisition of a full set of teeth to rapidly allow an efficient EVOLUTION Nesodon shows similar trends, but to a lesser extent, given that dentition for plant comminution.

Gomes Rodrigues et al. PNAS | January 31, 2017 | vol. 114 | no. 5 | 1071 Downloaded by guest on September 27, 2021 Correlated Dental Specializations and Structural Constraints. As dentitions for the Mesotheriidae and the Hegetotheriidae, and a clearly evidenced by the codistributions of character states (Fig. possible contemporaneous achievement of both features in 2), pairwise comparisons show a near-significant correlation (P = Toxodontidae may be proposed (Fig. 3A). In any case, it appears 0.0625; 252,144 pairings) (35) between the occurrence of ever- that, irrespective of the loose or strict temporal fit of their first growing cheek teeth and third molars erupting faster than occurrences, similar modifications of the eruption sequence sys- permanent premolars in notoungulates. However, even if ever- tematically accompany the convergent evolution of hypselodonty in growing teeth and modifications of the pattern of dental erup- notoungulates at some point in their history. tion show an almost perfectly replicated codistribution, some The striking and repeated combination of dental innovations differences still exist in their timing of appearance. The geo- observed in late diverging families of notoungulates has never logically earliest occurrence of this modified eruption sequence before been reported for mammals. It is worth mentioning that (i.e., faster eruption of third molars) was reported for Inter- extant ruminants encompass many species with high-crowned atheriidae and occurred during the Late (approximately teeth associated with fast eruption of molars, but their hyp- 35 Ma) (36, 37). This modification preceded a significant crown sodonty index is not significantly correlated with their eruption height increase in the clade (Fig. 3A). This pattern slightly pattern (12), as may also be assumed for the earliest interatheriid contrasts with other hypselodont notoungulate clades that pre- notoungulates. Nonetheless, inherent structural constraints may sent almost strictly replicated codistributions of ever-growing have facilitated these ontogenetic modifications in different cheek teeth and faster molar eruption (Fig. 2). In fact, although families of notoungulates. More precisely, the continuous in- it partly depends on the optimization of some undocumented or crease of crown height could have favored modifications of the polymorphic taxa, a slightly earlier acquisition of ever-growing dental eruption sequence by means of similar ontogenetic

Fig. 3. (A) Timing of appearance of main dental innovations in early diverging taxa and main groups of notoungulates and in selected South American mammals acquiring ever-growing dentitions (absolutes ages, 17). These data are compared with (B) climatic and geological variations in South America and (C) environmental variations in during the Cenozoic (14, 16, 28, 48).

1072 | www.pnas.org/cgi/doi/10.1073/pnas.1614029114 Gomes Rodrigues et al. Downloaded by guest on September 27, 2021 adjustments. In addition to lengthening the efficiency of the Conclusions dentition, increasing the duration of crown growth could al- Because the causes of changes in dental eruption pattern are low for postponing the time when teeth reach their maximal probably multiple and complex, it is surprising to observe these length (i.e., adult length) during a lifetime, conversely to low- repeated changes correlated with hypselodonty in notoungulates. crowned species for which the length is maximal as teeth This unique pattern therefore raises questions regarding the fac- appear. This delay has notably been observed in Neogene tors (e.g., structural or functional) that may have caused this Mesotheriidae and Toxodontidae, for which dental lengths phenomenon in late diverging notoungulates. However, even if are smaller in juveniles than in adults (34). Consequently, these taxa display some similar dental trends and specializations, more space should be available for the development of molar they also show important differences in other anatomical aspects. teeth at the back of the jaw in young notoungulates, even if These differences may reflect some ecological divergence, as the number of teeth in the jaw is not reduced (i.e., no di- expressed by their huge body mass variation and their relative astema), as in some Hegetotheriidae and Toxodontidae. This latitudinal partitioning (18). This assumption is substantiated by early development of molars was facilitated in derived spe- their diverse range of dental and cranial shapes (18, 20, 41), cies, such as some Hegetotheriidae and Mesotheriidae, hav- meaning that future research would benefit from a detailed in- ing a reduced dentition. Therefore, structural and ontogenetic vestigation of the mosaic evolution of their masticatory apparatus. trade-offs may also be partly responsible for the unique pattern of The study of dental patterns revealed not only that notoun- gulates convergently underwent similar morphological and on- correlated and convergent dental specializations observed in togenetic modifications, but it also provided crucial information notoungulates, possibly adding a further striking example of the on life history traits and ecology. However, the integration of major role played by these parameters on morphology (38). bone histology in addition to studies on dental ontogeny might be insightful to further characterize the evolution of South Correlated Dental Specializations in Constraining Environments. In- American mammals. In a broader context, such an integrative terestingly, some of the dental innovations, especially crown approach could provide new insights into the different guilds of height increase, contemporaneously occurred in notoungulates mammals evolving under strong environmental constraints. and other South American mammals, such as caviomorph ro- dents (e.g., Chinchilloidea, Cavioidea) and argyrolagoid marsu- Materials and Methods A pials (17) (Fig. 3 ). One might therefore hypothesize that most Dentition Analyses. Seventy taxa encompassing 69 notoungulates, and Trig- of these dental innovations were influenced by similar external onostylops (Astrapotheria) as the outgroup, were considered in this study. factors, because of their correlated and convergent occurrence, Data concerning dental eruption involved only cheek teeth (i.e., premolars and their close temporal proximity. Among them, the Andean and molars) and were obtained based on juvenile and adult specimens uplift in association with global cooling (Fig. 3B) may have partly housed in the Muséum National d’Histoire Naturelle (MNHN) (Paris), the driven increasing aridity in environments, as previously demon- Museo Argentino de Ciencias Naturales (MACN) (Buenos Aires), the Museo de La Plata (MLP) (La Plata, ), the American Museum of Natural strated for the southern part of South America since the Eocene History (AMNH) (New York), the Field Museum of Natural History (FMNH) (Fig. 3C). Strikingly, the main periods of crown height increase (Chicago), the Museo Nacional de Historia Natural (MNHN) (La Paz, Bolivia), and modification of the eruption sequence in notoungulates in- and from the literature (SI Appendix). Data concerning estimates of body cludes the main episodes of uplift intensification (i.e., Middle mass were mainly taken from Reguero et al. (31) and Croft (43). Additional Eocene, Early , and Early Miocene) (14). As also data were calculated following the protocol of Croft (43) based on upper suggested by Kohn et al. (30), such variations in volcanic activity first molar length (SI Appendix). Data concerning crown height of notoungulates were mainly taken from Billet (44) and a few additional and climate in South America may have slowly driven crown specimens (SI Appendix). height increase through the high abundance of dust adhering to plants ingested by notoungulates and other herbivorous mam- Construction of the Phylogenetic Tree and Character State Mapping. To trace mals eating plants occurring mainly close to the soil. the phylogenetic history and describe the evolutionary patterns of the in- Although it remains difficult to accurately evaluate the direct vestigated dental features, we constructed a composite cladogram for the influence of these external factors on the entire set of correlated notoungulates included in our study, based on recent phylogenetic studies dental innovations observed in notoungulates, we propose some (32, 44, 45) (SI Appendix). The scoring of discrete characters was undertaken ecological and physiological avenues to be explored. Among for the three features under scrutiny in this paper (SI Appendix): crown height, body mass, and modes of dental eruption, and for which three dis- factors leading to dietary changes, increasing aridity could have crete states were defined (Figs. 1 and 2). A parsimony reconstruction of at least triggered the emergence and abundance of new types of character evolution was performed using Mesquite version 3.04 (46) with a vegetation, such as shrublands observed in Patagonia during the Deltran optimization (47) for branches whose state was ambiguous. For each second part of the Paleogene (16, 29) (Fig. 3C), although forests reconstruction, we verified that the different optimizations did not affect probably remained dominant until the Middle Miocene in South the number of convergent events discussed in the text, i.e., only non- America (15, 39), especially in the northern part (14). Pending ambiguous convergent events were considered in the results. In addition, stratigraphic ranges for the simplified phylogeny (Fig. 3) were taken from more precise environmental data, it seems at least reasonable to Madden (17), and Reguero and Prevosti (45), except for divergences that assume that the acquisition of a more durable and rapidly effi- were located close to the first stratigraphic occurrence of taxa. cient dentition allowed notoungulates to widen the spectrum of plants consumed (19, 40, 41) in being more tolerant toward Statistics. The assessment of discrete character correlation (crown height vs. abrasives, which partly led to their subsequent specializations. dental eruption) was made using pairwise comparisons (choosing pairs These innovations may also have allowed juvenile notoungulates contrasting in states of two characters (SI Appendix) (35) in Mesquite version to exploit more rapidly an abundant and readily available food 3.04 (46). For this purpose, a less complete cladogram was used to avoid polytomies (incompatible with pairwise comparisons) and some taxa were type, which contributed to reducing the energetic cost of foraging pruned or relocated (SI Appendix). (42). This is the case of many extant fast-growing herbivores, such as ruminants and horses (2, 3), and may be assumed to be ACKNOWLEDGMENTS. We thank the curators B. Mamani Quispe (MNHN, La the case for notoungulates. Consequently, these combined dental Paz), A. Kramarz and S. Alvarez (MACN, Buenos Aires), M. Reguero (MLP), specializations could constitute markers of ecological and phys- Judith Galkin (AMNH), and William Simpson (FMNH), who allowed us to

access the paleontological collections of mammals and to publish pictures of EVOLUTION iological changes in notoungulates associated with a more con- specimens; D. Croft (Case Western Reserve University) for sending images of straining environmental context. notoungulate dentitions; M. Boivin (Institut des Sciences de l’Evolution de

Gomes Rodrigues et al. PNAS | January 31, 2017 | vol. 114 | no. 5 | 1073 Downloaded by guest on September 27, 2021 Montpellier) for interesting discussions on dental eruption in extinct Cavio- to improve this article. This work was supported by the LabEx BCDiv (Labo- morpha; and the editor and two anonymous reviewers, who greatly helped ratoire d’Excellence Biological and Cultural Diversities, labex-bcdiv.mnhn.fr/).

1. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17: 27. Billet G, Blondel C, de Muizon C (2009) Dental microwear analysis of notoungulates 462–468. (Mammalia) from Salla (Late Oligocene, Bolivia) and discussion on their precocious 2. Sibly RM, Brown JH (2007) Effects of body size and lifestyle on evolution of hypsodonty. Palaeogeogr Palaeoclimatol Palaeoecol 274:114–124. life histories. Proc Natl Acad Sci USA 104(45):17707–17712. 28. Armijo R, Lacassin R, Coudurier-Curveur A, Carrizo D (2015) Coupled tectonic evolu- 3. Sibly RM, Grady JM, Venditti C, Brown JH (2014) How body mass and lifestyle affect tion of Andean orogeny and global climate. Earth Sci Rev 143:1–35. juvenile biomass production in placental mammals. Proc Biol Sci 281(1777):20132818. 29. Strömberg CAE, Dunn RE, Madden RH, Kohn MJ, Carlini AA (2013) Decoupling the 4. Western D (1979) Size, life history and ecology in mammals. Afr J Ecol 17:185–204. spread of grasslands from the evolution of grazer-type herbivores in South America. 5. Chinsamy A, Hurum JH (2006) Bone microstructure and growth patterns of early Nat Commun 4:1478. mammals. Acta Palaeontol Pol 51(2):325–338. 30. Kohn MJ, et al. (2015) Quasi-static Eocene–Oligocene climate in Patagonia promotes 6. Martinez-Maza C, Alberdi MT, Nieto-Diaz M, Prado JL (2014) Life-history traits of the slow faunal evolution and mid-Cenozoic global cooling. Palaeogeogr Palaeoclimatol Miocene Hipparion concudense (Spain) inferred from bone histological structure. Palaeoecol 435:24–37. PLoS One 9(8):e103708. 31. Reguero MA, Candela AM, Cassini GH (2010) Hypsodonty and body size in rodent-like 7. Kurtén B (1953) On the variation and population dynamics of fossil and recent notoungulates. The Paleontology of Gran Barranca: Evolution and Environmental mammal populations. Acta Zool Fenn 76:1–122. Change Through the Middle Cenozoic of Patagonia, eds Madden RH, Carlini AA, 8. Janis CM, Fortelius M (1988) On the means whereby mammals achieve increased Vucetich MG, Kay RF (Cambridge University Press, Cambridge), pp 358–367. functional durability of their dentitions, with special reference to limiting factors. Biol 32. Townsend KEB, Croft DA (2010) Middle Miocene mesotheriine diversity at Cerdas, Rev Camb Philos Soc 63(2):197–230. Bolivia and a reconsideration of Plesiotypotherium minus. Palaeontol Electron 13(1): 9. Damuth J, Janis CM (2011) On the relationship between hypsodonty and feeding 1A:36p. ecology in ungulate mammals, and its utility in palaeoecology. Biol Rev Camb Philos 33. Billet G, Martin T (2011) No evidence for an afrotherian-like delayed dental eruption – Soc 86(3):733–758. in South American notoungulates. Naturwissenschaften 98(6):509 517. 10. Smith BH (1989) Dental development as a measure of life history in primates. 34. Patterson B (1952) Notas acerca del craneo de un ejemplar juvenil de Mesotherium – Evolution 43:683–688. cristatum Serr. Rev Mus Mun Cienc Nat Trad Mar del Plata 1:71 78. 11. Smith BH (2000) “Schultz’srule” and the evolution of emergence and re- 35. Maddison WP, FitzJohn RG (2015) The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst Biol 64(1):127–136. placement patterns in primates and . Development, Function and Evolution 36. Vera B, Cerdeño E (2014) New insights on Antepithecus brachystephanus Ameghino, of Teeth, eds Teaford MF, Smith MM, Ferguson MWJ (Cambridge University Press, 1901 and dental eruption sequence in ‘notopithecines’ (Mammalia, Notoungulata) Cambridge), pp 212–227. from the Eocene of Patagonia, Argentina. Geobios 47:165–181. 12. Veitschegger K, Sánchez-Villagra MR (2016) Tooth eruption sequences in cervids and 37. Vera B (2016) Phylogenetic revision of the South American notopithecines (Mam- the effect of morphology, life history, and phylogeny. J Mamm Evol 23:251–263. malia: Notoungulata). J Syst Palaeontology 14(6):461–480. 13. Godfrey LR, Samonds KE, Wright PC, King SJ (2005) Schultz’s unruly rule: Dental de- 38. Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian par- velopmental sequences and schedules in small-bodied, folivorous lemurs. Folia adigm: A critique of the adaptationist programme. Proc R Soc Lond B Biol Sci Primatol (Basel) 76(2):77–99. 205(1161):581–598. 14. Hoorn C, et al. (2010) Amazonia through time: Andean uplift, climate change, 39. Palazzesi L, Barreda V (2012) Fossil pollen records reveal a late rise of open-habitat landscape evolution, and biodiversity. Science 330(6006):927–931. ecosystems in Patagonia. Nat Commun 3:1294. 15. Croft DA (2001) Cenozoic environmental change in South America as indicated by 40. Mac Fadden BJ (2005) Diet and habitat of toxodont megaherbivores (Mammalia, mammalian body size distributions (cenograms). Divers Distrib 7:271–287. Notoungulata) from the late of South and Central America. Quat Res 64: 16. Dunn RE, Strömberg CAE, Madden RH, Kohn MJ, Carlini AA (2015) Linked canopy, 113–124. – climate, and faunal change in the Cenozoic of Patagonia. Science 347(6219):258 261. 41. Cassini GH (2013) Skull geometric morphometrics and paleoecology of 17. Madden RH (2015) Hypsodonty in Mammals: Evolution, Geomorphology, and the (Late Early Miocene; Patagonia) native ungulates (Astrapotheria, , and Role of Earth Surface Processes (Cambridge University Press, Cambridge), p 423. Notoungulata). Ameghiniana 50:193–216. 18. Simpson GG (1980) Splendid Isolation: The Curious History of South American 42. Clauss M, Steuer P, Müller DW, Codron D, Hummel J (2013) Herbivory and body size: Mammals (Yale University Press, New Haven, CT). Allometries of diet quality and gastrointestinal physiology, and implications for 19. Shockey BJ, Croft DA, Anaya F (2007) Analysis of function in the absence of extant ecology and dinosaur gigantism. PLoS One 8(10):e68714. functional homologues: A case study of mesotheriid notoungulates. Paleobiology 33: 43. Croft DA (2000) (Mammalia: Notoungulata) from the Tinguiririca – 227 247. Fauna, central Chile, and the evolution and paleoecology of South American mam- 20. Giannini NP, García-López DA (2014) Ecomorphology of mammalian fossil lineages: malian herbivores. PhD dissertation (University of Chicago, Chicago). Identifying morphotypes in a case study of endemic South American ungulates. 44. Billet G (2011) Phylogeny of the Notoungulata (Mammalia) based on cranial and J Mamm Evol 21:195–212. dental characters. J Syst Palaeontology 9(4):481–497. 21. Stebbins GL (1981) Coevolution of grasses and herbivores. Ann Mo Bot Gard 68:75–86. 45. Reguero MA, Prevosti FJ (2010) Rodent-like notoungulates (Typotheria) from Gran 22. MacFadden BJ (2000) Cenozoic mammalian herbivores from the Americas: Re- Barranca, Chubut Province, Argentina: phylogeny and systematics. The Paleontology constructing ancient diets and terrestrial communities. Annu Rev Ecol Syst 31:33–59. of Gran Barranca: Evolution and Environmental Change Through the Middle Ceno- 23. Pascual R, Ortiz-Jaureguizar E (1990) Evolving climates and mammal faunas in zoic of Patagonia, Chapter 10, eds Madden RH, Carlini AA, Vucetich MG, Kay RF Cenozoic South America. J Hum Evol 19:23–60. (Cambridge University Press, Cambridge), Vol 152–169. 24. Jardine PE, Janis CM, Sahney S, Benton MJ (2012) Grit not grass: Concordant patterns 46. Maddison WP, Maddison DR (2015) Mesquite: A modular system for evolutionary of early origin of hypsodonty in Great Plains ungulates and . Palaeogeogr analysis, Version 3.04. Palaeoclimat Palaeoecol 365–366:1–10. 47. Agnarsson I, Miller JA (2008) Is ACCTRAN better than DELTRAN? Cladistics 24: 25. Buckley M (2015) Ancient collagen reveals evolutionary history of the endemic South 1032–1038. American ‘ungulates’. Proc Biol Sci 282(1806):20142671. 48. Cramer BS, Toggweiler JR, Wright JD, Katz ME, Miller KG (2009) Ocean overturning 26. Welker F, et al. (2015) Ancient proteins resolve the evolutionary history of Darwin’s since the Late : Inferences from a new benthic foraminiferal South American ungulates. Nature 522(7554):81–84. isotope compilation. Paleoceanography 24:PA4216.

1074 | www.pnas.org/cgi/doi/10.1073/pnas.1614029114 Gomes Rodrigues et al. Downloaded by guest on September 27, 2021