Virtual cranial endocast of Lotheridium mengi and brain evolution in early metatherians

Very little is known about the early brain evolution of Metatheria, and no brain endocast of this group has been described from prior to the Cretaceous-Paleogene (K-Pg) boundary. This has led to great uncertainty regarding the ancestral condition of the therian brain. Here, we aim to fill some of this gap by describing the first brain endocast of a Cretaceous metatherian, Lotheridium mengi from the Late Cretaceous of Henan, China. Lotheridium has an encephalization quotient comparable to the Cretaceous multituberculate Chulsanbaatar and eutherian Asioryctes and reaches the lower range of crown mammals. Together with patterns observed in other Mesozoic mammals, this suggests that increased encephalization evolved independently in several major mammalian lineages. The endocast is characterized by relatively small olfactory bulbs, well-developed petrosal lobules, and a prominent hypophyseal cast, differentiating it from earlier mammals. With the addition of a dorsally exposed midbrain, Lotheridium closely resembles the condition observed in Cretaceous eutherians. We propose that reduced olfactory bulb proportions and increased endocranial volume in Cretaceous eutherians and metatherians reflect a major shift in mammalian brain evolution, from primarily olfactory bulb expansion in the Jurassic to predominantly neocortical, brainstem, and cerebellar expansion in the Late Cretaceous. The endocranial morphology of Lotheridium further indicates that several neuroanatomical features characteristic of Paleogene and extant marsupials, including relatively enlarged olfactory bulbs and a smaller brain size compared to eutherians, are unlikely to represent the plesiomorphic condition for Metatheria. Ultimately, Lotheridium provides crucial new information regarding the ancestral condition of marsupial brains.