The origin of placental mammal life histories

Abstract

After the end-Cretaceous extinction, placental mammals quickly diversified 1 , occupied key ecological niches 2,3 , and increased in size 4,5 , but the latter was not true of other therians 6 .The uniquely extended gestation of placental young 7 may have factored in their success and size increase 8 , but reproduction style in early placentals remains unknown. Here, using palaeohistology and geochemistry, we present the earliest record of a placental life history, 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 mapping 9,10 by sixty million years, identifying chemical markers of birth and weaning, and calibrate these to a daily record of growth in the dentition. A long gestation (~7 months), rapid dental development, and short suckling interval (~30-75 days) show Pantolambda bathmodon was highly precocial, unlike non-placental mammals and known Mesozoic precursors. These results demonstrate P. bathmodon reproduced like a placental, and lived at a fast pace for its body size. Assuming P. bathmodon reflects close placental relatives, our findings suggest 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.Placentals are the most diverse group of mammals, comprising >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 3 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-Ma lineage of small-bodied ancestors and quickly achieved much greater masses as they diversified into a variety of niches 4 . Thus, the early Palaeocene was likely 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 (~62 ma) Pantolambda bathmodon (~42 kg) is represented by multiple skel...

The longevity bottleneck hypothesis: Could dinosaurs have shaped ageing in present‐day mammals?

“…Silhouettes from phylopic.org. they have been estimated to have a shorter lifespan than expected for their body size, [36] which in light of the longevity bottleneck hypothesis is tempting to speculate resulted from their evolution from small, short-lived ancestors.…”

“…[ 32 ] By contrast, abundant fossil and phylogenetic evidence shows that after the Cretaceous–Paleogene extinction event there was a rapid diversification and increase in mammalian body size, [ 33–35 ] which one study estimated levelled off 40 mya. [ 31 ] Interestingly, pantodonts, the first mammals 62 mya to achieve a large size (∼42 kg) lived at a fast pace as they have been estimated to have a shorter lifespan than expected for their body size, [ 36 ] which in light of the longevity bottleneck hypothesis is tempting to speculate resulted from their evolution from small, short‐lived ancestors.…”

Elemental models of primate nursing and weaning revisited

“…The choice of element is not without debate; we have argued that Ba/Ca measurements are more informative about the initiation and duration of suckling (e.g., Austin et al, 2013;Smith et al, 2021Smith et al, , 2022, while others have suggested that Sr/Ca distributions are more accurate (e.g., Li et al, 2020;Müller et al, 2019;Nava et al, 2020). Such explorations have also been extended into other mammals; Clark et al (2020) conducted an elemental study of early-formed walrus teeth, revealing Ba and Sr decreases that are consistent with the Ba/Ca nursing model developed by Austin et al (2013) but inconsistent with the Sr/Ca model proposed by Humphrey, Dirks, et al (2008). Funston et al (2022 documented nursing transitions from Ba-rich regions in the molars of a 62 million-year-old pantodont, providing key insight into this enigmatic placental mammal.…”

“…Such explorations have also been extended into other mammals; Clark et al ( 2020 ) conducted an elemental study of early‐formed walrus teeth, revealing Ba and Sr decreases that are consistent with the Ba/Ca nursing model developed by Austin et al ( 2013 ) but inconsistent with the Sr/Ca model proposed by Humphrey, Dirks, et al ( 2008 ). Funston et al ( 2022 ) documented nursing transitions from Ba‐rich regions in the molars of a 62 million‐year‐old pantodont, providing key insight into this enigmatic placental mammal.…”

A labeling study of dentin formation rates during crown and root growth of porcine mandibular first molars

“…Establishing dental growth parameters is a crucial part of comparative biological research aiming at elucidating life history traits of both, extant and extinct mammals. This approach can provide insights into adaptations of developmental processes that have occurred during the evolutionary history of a species, including changes in the course of domestication (Dean, 2010; Dean et al, 2020; Dirks et al, 2009; Emken et al, 2023; Funston et al, 2022; Jordana et al, 2014; Le Cabec et al, 2017; Modesto‐Mata et al, 2020; Nacarino‐Meneses et al, 2017; Nacarino‐Meneses & Chinsamy, 2021; O'Meara et al, 2018). A knowledge of the growth rates of dental hard tissues is also decisive for the reconstruction of the timing of stress events affecting tooth formation.…”