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The Rise of Placental Mammals: Dissecting an Evolutionary Radiation

Periodic Reporting for period 4 - PalM (The Rise of Placental Mammals: Dissecting an Evolutionary Radiation)

Reporting period: 2022-07-01 to 2023-12-31

Mammals are ubiquitous in today’s world. Over 5,000 species, from hamsters to humans, are distributed across the globe. But how did mammals become so successful? This question gets to the heart of a much wider mystery: how major groups of plants and animals rise up over evolutionary time. How do their evolutionary radiations unfold: when do they happen, how quickly, and what drives them? Answering these questions will help us better understand how major groups become successful over evolutionary time and how biodiversity is affected by large, infrequent events like mass extinctions. It will also give unique insight into the early stages of our own evolutionary story.

Two main handicaps have held back generations of researchers. First, tackling the mystery of the mammal radiation requires multiple lines of evidence that transcend traditional research boundaries. Second, we still know very little about those mammals that flourished during the ~10 million years after the end-Cretaceous extinction (the early Paleogene). They are often ignored, because they mostly belong to ‘archaic’ groups, with uncertain relationships to both Cretaceous and modern mammals. How to place these ‘archaic’ species—some 200+ species of incredible anatomical, dietary, and body size diversity— on the family tree of mammals is one of the great unsolved problems in palaeontology.

A wealth of new fossils (including specimens collected over the past decade by our team) and new multidisciplinary analytical techniques together provide an unprecedented opportunity to untangle the biology and phylogeny of these critical early Paleogene species, and then to use that information to better understand how mammals ascended to dominance and what role the end-Cretaceous extinction played in this story. In doing so, our team integrated, for the first time, a wealth of data on the anatomy, genetics, ages, genealogy, and body sizes of early mammals and their modern relatives, providing the most detailed look yet at a major evolutionary radiation in the fossil record.

Detailed Objectives:
1) What are the genealogical relationships of Paleogene mammals: how are they related to each other and to their Cretaceous forebears and living mammals? We tested whether some/all ‘archaic’ Paleogene species are early members of major living mammal groups, failed experiments in mammalian evolution that did not produce any descendants, and/or linked to Cretaceous species that lived alongside the dinosaurs.
2) When did placental mammals and major subgroups originate? We tested the time component of the three main hypotheses for placental diversification—explosive, long-fuse, and short-fuse—and determine which best fits the available data, thus establishing whether placentals and major subgroups originated alongside, or after the extinction of, dinosaurs.
3) What effect did the end-Cretaceous extinction have on mammalian evolution? We tested the rate component of the three main hypotheses for placental diversification, and determine whether there were changes in biodiversity across the Cretaceous-Paleogene boundary, whether the extinction preferentially wiped out certain types of mammals, and how mammals emerged from the extinction and radiated to become the diverse animals we know today.
PI Brusatte built his research team in Edinburgh, which included three PhD students and three postdocs. Our team held four meetings: Pittsburgh (USA) in March 2019, Albuquerque (USA) in May 2019, Edinburgh in April 2022 and April 2023. We visited key museum collections and conducted fieldwork in New Mexico that recovered ca. 150 new specimens of Paleocene mammal fossils. We obtained computed tomography (CT) scans of 50+ fossil mammal skulls. Some other planned meetings, data collections trips, and joint work with our colleagues was cancelled because of the Covid-19 pandemic.

Our main achievements include: 18 peer-reviewed papers (including in Science, Nature and PNAS), 30+ papers (talks or posters) presented at major international conferences, ca. 80 talks (academic and popular) by PI Brusatte, three major popular science articles by PI Brusatte (a cover article for Scientific American, two articles including one cover article for BBC Science Focus Magazine), and a major pop science book by PI Brusatte (The Rise and Reign of the Mammals, 2022). We have finished our full dataset of anatomical and genetic data for extinct and extant mammals to be used for phylogenetic analysis, and this will form the basis for additional work continuing beyond the timescale of this grant.
First, we constructed the largest and most comprehensive dataset to date for building a family tree of extinct and modern placental mammals. Our dataset includes anatomical information on Paleocene placentals along with older and younger fossil and modern mammals. We assessed a total of 209 species for 2547 anatomical features, for a total of 532,323 unique observations. To this, we added 14 mitochondrial genes, 26 nuclear genes, and two amino acid sequences for 44 modern mammals. Our combined fossil + modern and molecular + morphological dataset is of a size and scope that far surpasses any previous dataset. Because of delays in visiting museums to collect data during the Covid-19 pandemic, we finished our dataset just as the grant was ending, so we will publish it shortly, although we presented a preliminary version at the 2022 Society of Vertebrate Paleontology meeting.

Second, we demonstrated that, contrary to decades of consensus that mammal brains have increased incrementally over time, Paleocene species initially reduced their relative brain sizes because of a higher rate in body mass increase. Later, during the Eocene, several modern placental groups independently acquired relatively large brains through the growth of sensory regions, particularly the neocortex, associated with keener sensory integration. Paleocene placentals initially increased in body size as the survivors from the end-Cretaceous extinction filled vacant niches, but then the brain became larger as ecosystems started to saturate and competition intensified among archaic and modern placentals in the Eocene.

Third, we used paleohistology, scanning electron microscopy, and geochemical analyses on fossils to reconstruct diets, age, and growth patterns. The keystone result was reconstruction of the life history of Pantolambda, a ~62 million-year-old Paleocene placental, using histological analysis of bones and teeth combined with high-resolution analysis of dental trace element concentrations of zinc and barium that are correlated with birth, suckling milk, and weaning to solid foods in living mammals. This study extended the viability of trace element analysis in fossil teeth by an order of magnitude; the previous state-of-the art study had found these chemical signatures in the teeth of two-million-year-old human ancestors. We demonstrated that Pantolambda had a placental-like reproduction with a long gestation period in the womb (7 months) followed by a short time drinking its mother’s milk (31-75 days). This is the oldest evidence for a placental-style reproduction in any mammal, and we hypothesized that this pattern of reproduction (particularly the ability to raise babies long in the womb and thus give birth to larger young) was the key that allowed some Paleocene placental mammals to reach large body sizes quickly after the end-Cretaceous extinction.
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