The origin of placental mammal life histories

After the end-Cretaceous extinction, placental mammals quickly diversified1, occupied key ecological niches2,3 and increased in size4,5, but this last was not true of other therians6. The uniquely extended gestation of placental young7 may have factored into their success and size increase8, but reproduction style in early placentals remains unknown. Here we present the earliest record of a placental life history using palaeohistology and geochemistry, in a 62 million-year-old pantodont, the clade including the first mammals to achieve truly large body sizes. We extend the application of dental trace element mapping9,10 by 60 million years, identifying chemical markers of birth and weaning, and calibrate these to a daily record of growth in the dentition. A long gestation (approximately 7 months), rapid dental development and short suckling interval (approximately 30–75 days) show that Pantolambda bathmodon was highly precocial, unlike non-placental mammals and known Mesozoic precursors. These results demonstrate that P. bathmodon reproduced like a placental and lived at a fast pace for its body size. Assuming that P. bathmodon reflects close placental relatives, our findings suggest that the ability to produce well-developed, precocial young was established early in placental evolution, and that larger neonate sizes were a possible mechanism for rapid size increase in early placentals. Using palaeohistology and geochemistry, the placental-like life history of a pantodont species 62 million years of age is determined.

Placentals are the most diverse group of mammals, comprising more than 6,000 extant species 11 and the largest animals ever. Their success may relate to their derived life history 8,12 , with maternal investment shifted prenatally through extended gestation 7,13 . This adaptation allows placentals the unique capability among mammals to produce highly precocial young: typically single offspring born at larger masses with well-developed dentition, fur and open eyes 13,14 . Extended gestation may have released placentals from developmental constraints associated with prolonged lactation in other mammals 8,15,16 , enabling experimentation with new locomotor modes and habitats 17,18 . However, when extended gestation evolved in mammals remains unclear; Mesozoic eutherians (mammals more closely related to placentals than marsupials) did not grow like living placentals [19][20][21] and it has been hypothesized that ancestral placentals gave birth to altricial young 21 . Nonetheless, immediately after the end-Cretaceous extinction, early Palaeocene placentals emerged from a 100 million years ago (Ma) lineage of small-bodied ancestors and quickly achieved much greater masses as they diversified into various niches 4 . Thus, the early Palaeocene was probably an important interval in the eutherian transition to placental-like growth strategies, but the life histories of these mammals remain unknown.
Among early placental clades, the Palaeocene-Eocene Pantodonta are a key group, because they were among the first large mammalian herbivores, becoming the largest mammals ever up to that point in time 22 . The early Palaeocene (approximately 62 Ma) P. bathmodon (approximately 42 kg) is represented by multiple skeletons representing most of its ontogeny, including a small juvenile with deciduous dentition and unfused epiphyses (New Mexico Museum of Natural History and Science (NMMNH) P-27844; approximately 17 kg at death). As one of the largest mammals in its ecosystem 23 , its life history might provide insight into the relationship between life history and body size in Palaeocene eutherians.
Life histories of extinct animals can be reconstructed using incremental growth features of mineralized tissues such as bones and teeth [24][25][26] . Bones preserve evidence of stress and annual cycles 27,28 , and they accurately reflect growth rate throughout life 29,30 , including changes associated with maturity 31 . In teeth, daily incremental lines in the dentine and enamel allow for precise chronologies and faithful recording of life history events including birth and nutritional stress such as that experienced during weaning 32,33 , whereas cementum preserves annual growth cycles 24,34 . Chemical signals of birth and early-life diet are recorded in the developing teeth by the abundances of certain trace elements, such as zinc (Zn), which is enriched at birth 35,36 , and barium (Ba), which varies according to bioavailability in the diet 26 . When integrated with daily growth increments, trace element maps can reveal birth and the timing of weaning, a technique applied to primates up to 2.6 million years of age 9,10,26 , but with unrealized potential in other fossil mammals.
Here we combine palaeohistological and geochemical evidence to reconstruct the life history of P. bathmodon on a daily scale and evaluate the physiology of a key group in the rise of mammals following the end-Cretaceous mass extinction. These data provide unprecedented insight into the life history of a fossil mammal, revealing that characteristic placental reproductive strategies were established early in their evolution.

Dental development, birth and weaning
Incremental growth features are well preserved in the teeth, especially the enamel, and are clearly visible in histological thin sections ( Fig. 1b-g and Extended Data Fig. 1). Daily laminations in the dentine and enamel 37 (Fig. 1b,c,e) track the successive growth of the tooth crown (Extended Data Table 1). High-resolution trace element mapping of several teeth (Extended Data Table 1 and Supplementary Figs. 1-7) reveals patterns in Zn and Ba that correspond to these incremental growth patterns and provide evidence of birth and weaning in P. bathmodon (Fig. 2), extending the viable window for dietary trace element mapping by roughly 60 million years compared with previous studies 10 . The most complete record of early life comes from a second lower molar of an adult individual (NMMNH P-19541), in which both the neonatal event and the weaning transition are preserved (Fig. 2).
Birth is recorded in the enamel by a prominent neonatal line (Figs. 1g and 2b), a discontinuity in the enamel prisms reflecting developmental disruptions in response to the physiological stress of birth 38 . The neonatal line is Zn-enriched ( Fig. 2b and Extended Data Fig. 2), as observed in modern teeth, in which this results from changing levels of Zn in serum over the birth interval and the ingestion of Zn-rich colostrum 35,36 . The neonatal line is Zn-enriched in multiple cusps of the tooth, and no other accentuated lines in the enamel of this or other teeth are Zn-enriched ( Fig. 2b; see Supplementary Information). This suggests that analysis of Zn may be useful as an independent criterion for distinguishing neonatal lines from other accentuated lines in fossil mammals 36 .
Concentrations of Ba in the enamel were elevated postnatally, but decrease sharply after a short period (Fig. 2c). This pattern is present in both the protoconid and the paraconid of the second lower molar, as well as in the first lower molar of the same individual (Fig. 2d), indicating  that it represents a consistent biogenic signal. Temporary postnatal Ba enrichment in P. bathmodon is identical to that reported in modern and fossil primates 9,10,26 , in which it reflects the increased bioavailability of Ba in breastmilk 26 . The decreased levels in Ba presumably mark the onset of weaning and indicate a minimum suckling period of about 31-56 days in P. bathmodon. Further independent evidence for a short suckling period also comes from mesowear and microwear in the dentition of a young juvenile (NMMNH P-27844; Extended Data Fig. 3), where growth increments in the dentine of the deciduous teeth are exceptionally well preserved ( Fig. 1c and Extended Data Fig. 1). Like in the enamel, a birth signature appears to be recorded in the dentine by a neonatal line, and in this individual, the postnatal dentine is Zn-enriched (Extended Data Fig. 4). Dentine continues to infill the pulp cavity throughout life, providing a record of growth both before and after eruption of the tooth and allowing precise estimation of age at death 24 . Approximately 75 daily growth increments separate the neonatal line and the pulp cavity in each tooth of this juvenile skeleton, indicating an age at death of approximately 2.5 months for this individual. Despite its young age, the presence of dental mesowear and microwear 39 (Extended Data Fig. 3) in this individual shows that solid foods (not only milk) were being ingested, providing an upper constraint of 75 days on the onset of weaning.
Aligning daily growth records in the teeth based on the neonatal lines enabled the reconstruction of a dental chronology (Fig. 1l). Crown formation times in the teeth were rapid, ranging from 68 to 183 days (approximately 2-6 months; Extended Data Table 1). All of the deciduous teeth were complete and began erupting before birth, and the first and second adult molars had begun mineralizing. The adult molar crowns were completed within 4 months after birth and would have begun erupting in the first year. On the basis of the eruption sequences in other pantodonts [40][41][42] , in which the third molar erupts last, it is therefore likely that all of the adult teeth of P. bathmodon erupted within the first year (see Supplementary Information).
In the permanent teeth of mammals, age at death can be estimated from annual bands in the cementum that anchors the tooth to the jaw 24,34 . Cementum annulations were clearly present in the acellular cementum of most teeth in our sample (Fig. 1d). Most individuals had between two and four annual pairs (Extended Data Table 1), but three individuals with highly worn dentitions compared with other Palaeocene pantodonts had five, seven and possibly as many as 11 pairs, respectively (Extended Data Fig. 5; see Supplementary Information).

Skeletal growth
The bone microstructure of the juvenile skeleton (NMMNH P-27844) exhibits densely vascularized fibrolamellar bone, indicating relatively rapid growth (Fig. 1i-k). No annual growth marks are present, consistent with its dental age of approximately 2.5 months, but a band of more organized, slowly growing parallel-fibred bone occurs towards the outer surface of the radius and tibia (Fig. 1i and Extended Data Fig. 6), at an estimated mass of 9 kg (see Supplementary Information). External to this band, the bone shows reduced vascularity and relatively slower growth, on the basis of a higher proportion of parallel-fibred matrix (Fig. 1j,k), although laminations in this tissue are not as well developed as in the lamellar bone of the adult individual. This transition probably corresponds to changes in growth rate associated with weaning, as in living ungulates, a similar transition occurs in some individuals over this interval 43 (see Supplementary Information). The position of this transition partway through the cortex provides evidence for weaning in this individual before death at 2.5 months of age, supporting the 1-2 month suckling period suggested by dental trace elements and tooth wear.
In a skeletally mature adult (NMMNH P-22012), seven annual growth marks were discernible in the exterior cortical bone, matching the number of cementum annulations in its teeth and demonstrating that it was 7 years of age when it died. The exterior cortex is formed of highly organized lamellar bone, indicating slow growth (Fig. 1h). The earliest annual growth mark is within the slowly growing exterior cortex (Extended Data Fig. 7), indicating that growth rate decreased substantially before the end of the first year of life. This probably corresponds to the achievement of sexual maturity 31 , suggesting that P. bathmodon probably reached sexual maturity and approached maximum body size in its first year.

Life history in P. bathmodon
Correcting for the onset of tooth mineralization partway through fetal development (see Supplementary Information), the prenatal growth record in the deciduous teeth indicates a gestation period of roughly 207 days or 29.5 weeks. This is an order of magnitude longer than in marsupials or monotremes, but falls close to extant placentals of similar body size (Fig. 3b). Within placentals, gestation length is dichotomous between species that give birth to single or multiple young in each litter 44 (Fig. 3c). The long gestation period in P. bathmodon suggests that it was likely (posterior probability = 0.96) to have given birth to singleton offspring (see Supplementary Information).
Multiple independent lines of evidence from two individuals indicate the onset of weaning between 1 and 2 months after birth in P. bathmodon. Postnatal enrichment in enamel Ba for 1-2 months after birth in an adult individual (Fig. 2c,d) is consistent with the development of abrasive microwear and mesowear on the dentition of the juvenile 2.5 months of age (Extended Data Fig. 3) and with the transition recorded in its limb bones (Extended Data Fig. 6), identical to weaning transitions recently described on the basis of fluorescent labelling 43 . Together, these lines of evidence constrain weaning in P. bathmodon to between 31 and 75 days after birth, with the weight of evidence supporting cessation of suckling by 2 months after birth. The age (31-75 days) and mass (9 kg) at Article weaning in P. bathmodon were shorter and smaller than expected for a placental of its adult body mass, but its gestation period (207 days) was slightly longer (Fig. 3a,b). This indicates greater prenatal than postnatal investment in the young, characteristic of placental mammals 7 , but also suggests a distinct life history for these early Palaeocene placentals, consistent with other unusual aspects of their biology 45 .
Most individuals within our sample died between 2 and 5 years of age (Fig. 1l), suggesting high mortality in young animals. The oldest specimen in our sample (estimated to be approximately 11 years of age) lived only half the expected lifespan for a mammal of its body mass (20 years; Fig. 3d). This high mortality, in conjunction with its short suckling period and rapid onset of sexual maturity (Fig. 3a,e), suggests a fast pace of life in P. bathmodon, despite its relatively large size (42 kg).
Combined with its rapid dental and skeletal development, these life history parameters indicate a highly precocial lifestyle in P. bathmodon, comparable with the most precocial extant mammals (for example, deer, giraffes and sheep), which give birth to young with hair and open eyes 13,14 . After a long gestation-the hallmark of the typical placental reproductive mode-a mother P. bathmodon probably gave birth to a single, haired offspring with open eyes and well-developed dentition, which was nursed for 1-2 months. At approximately 62 Ma, this constitutes the earliest example of a placentalian-grade physiology in the fossil record.

Growth in early placentals
The growth pattern and rate of P. bathmodon differs from those of both Mesozoic mammaliaforms 19,34 and other Cenozoic mammals 46,47 . The mammaliaform Morganucodon grew at a much slower rate and for a longer period, evidence of a protracted life history more like that of reptiles than of mammals 19,34 . Late Cretaceous multituberculates and some eutherians had faster growth rates than Morganucodon, but these were still not as rapid as extant mammals 19 . By contrast, P. bathmodon exhibits fast growth rates and a rapid developmental schedule, more similar to living precocial placentals. Nonetheless, P. bathmodon lived and died faster than expected for a mammal of its body size, outpacing extant mammals and even other extinct mammals from later in the Cenozoic 46,47 . The closest living analogues for Pantolambda, independent of mass (Extended Data Fig. 8a), are small antelope, such as the neotragines Madoqua (Dik-dik) and Raphicerus (Steenbok). However, when adult body mass is considered, Pantolambda is unique among terrestrial mammals (Extended Data Fig. 8b). This life history strategy would have enabled P. bathmodon to proliferate at a rapid rate for an animal of its size, which may have been advantageous in the recovering ecosystems of the Palaeocene. Perhaps, as was the case with locomotion 45 and brain size 48 , placental life history strategies became limited to their modern range later, as ecosystems saturated.
In contrast to its distinctly rapid pace of life, the gestation period of P. bathmodon is remarkably similar to living placentals of its body mass ( Fig. 3b and Extended Data Fig. 8), suggesting a more constrained relationship between size and gestation. Indeed, neonate weight and adult body mass are more tightly correlated than other life history parameters in extant placentals (Extended Data Fig. 9), suggesting that neonate weight drives and/or is constrained by adult body mass. As longer gestation enables the larger neonate sizes required for larger  Fig. 9c), extended gestation periods such as that in P. bathmodon may have contributed to the rapid increase in body mass in early Palaeocene placentals. The option of extended gestation may have reduced developmental constraints on body size and allowed placentals to expand into vacant niches after the extinction of the non-avian dinosaurs, reaching larger sizes than any Mesozoic mammal 22 and culminating in the largest animals ever 49 .

adults (Extended Data
The excellent preservation of daily incremental structures and dietary trace element signatures in a fossil approximately 62 million years of age unlock a new perspective for studying the life history of extinct mammals. Our results suggest that biogenic trace element signals can be retained much longer than previously realized, providing new tools for inferring birth and early-life diet in ancient fossil mammals. Rather than being a limitation for studying reproduction, the abundantly preserved isolated teeth of Mesozoic mammals may enable combined palaeohistological and geochemical approaches to directly address the evolution of reproduction in mammals, including its role in their survival at the end-Cretaceous extinction and their radiation thereafter. Indeed, the highly precocial life history of P. bathmodon shows that the physiology of at least some close placental relatives had diverged from other mammals by at least the Palaeocene, early in their evolutionary history 21 , and suggests that the capacity to increase body size had a role in their ascent from humble Mesozoic beginnings to the dominant role they have in global ecosystems today.

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