Rise of placental mammals: the anatomy and phylogeny of the South American native ungulates with a focus in the order Litopterna
Item statusRestricted Access
Embargo end date23/05/2024
Puschel, Hans P.
Placentals are the most preeminent mammalian lineage today in terms of diversity and distribution over the world, having over 6000 recognised extant and recently extinct species. The timing for the origin and diversification of Placentalia, and its relationship with the Cretaceous-Palaeogene (K/Pg) mass extinction event, is one of the key questions in palaeontology. Different hypotheses have been proposed over the years for the inter and intraordinal diversification of placentals, each one with a distinct time and a rate component that make them identifiable if tested. Testing these hypotheses has been hindered by the limited knowledge of the “archaic” Palaeogene placental mammals that lived after the K/Pg mass extinction event. Among “archaic” Palaeogene mammals from different landmasses, those from South America stand out because of their particular biogeographic history. Indeed, it is only after the K/Pg mass extinction event that eutherians are found in the South American fossil record, probably the result of crossing in a single or multiple events from North America in the latest Cretaceous or early Palaeogene. Among these mammalian immigrants, there were placentals that gave rise to endemic groups, including Xenarthra and five or maybe six ancient “ungulate” orders known as the South American Native Ungulates (SANUs): Xenungulata, Notoungulata, Litopterna, Pyrotheria, Astrapotheria, and Notopterna (the latter usually included within Litopterna). SANUs were first discovered by Charles Darwin in the 19th century who immediately was puzzled by their bizarre anatomy, a feeling shared by Richard Owen one of the most prominent comparative anatomists of all time. To these “ungulate” orders a couple of families/subfamilies of “condylarths” (i.e., a wastebasket group of “archaic” ungulates) can be added: Didolodontidae, traditionally linked to Litopterna, and Kollpaninae, considered to be part of Mioclaenidae, a group of primitive ungulates otherwise known from North America. Interestingly, two SANUs orders, Litopterna and Astrapotheria, crossed from South America to Antarctica probably at some point between the late Palaeocene and the early Eocene. The phylogenetic position of the SANUs in the placental tree has been controversial over the years, but recently thanks to molecular evidence it was determined that Notoungulata and Litopterna are sister taxa, and that both are closely related to Perissodactyla (the odd-toed hoofed mammal group including horses and rhinos). However, how the rest of SANUs fit in the placental tree, and if SANUs effectively form a monophyletic group (i.e., Meridiungulata) are still open questions. In order to resolve the affinities of SANUs in the placental tree and the timing of their diversification, we first have to understand and determine the composition and affinities of each one of the SANU orders. Much research attention has been already given to the most diverse SANU order, Notoungulata, in detriment of the second most diverse order, Litopterna. Therefore, the main goal of this thesis is to determine the interfamilial relationships within Litopterna and the timing of its familial diversification. In order to achieve this goal, a deep understanding of modern phylogenetic methods and litoptern anatomy must be marshalled. Therefore, in Chapter 2 I first applied cutting-edge Bayesian phylogenetic methods to a case study, estimating the divergence-times of hominins and exploring trends in human evolution. Quantifying speciation times during evolution is fundamental as it provides a timescale to test for the correlation between key evolutionary transitions and extrinsic factors like climatic or environmental change. I applied a Total Evidence Dating approach for the first time to a hominin phylogeny to estimate divergence times under different topological hypotheses. The time scaled phylogenies were subsequently used to perform ancestral state reconstruction of body mass and phylogenetic encephalization quotient (PEQ), an index that determines relative brain size considering body mass and phylogeny. The divergence time estimates are consistent with other recent studies that analysed extant species. The origin of Homo most likely occurred between 4.30 and 2.56 Ma. The ancestral state reconstructions show a general trend towards a smaller body mass before the emergence of Homo, followed by a trend towards a greater body mass within Homo. PEQ estimations display a general trend of gradual but accelerating evolution of larger brain sizes relative to body sizes over time (i.e., encephalization). The obtained results provide a rigorous temporal framework for human evolution. In addition, this chapter allowed me to test the impact that different interpretations of the phylogenetic affinities of a lineage have in the divergence-time estimations for the different species within that lineage, which is particularly important in the phylogeny of litopterns considering how uncertain their early affinities are. In Chapter 3 I describe a new macraucheniine macraucheniid litoptern, Micrauchenia saladensis gen. et sp. nov. from the late Miocene (Huayquerian SALMA) and applied some of the phylogenetic methods described in chapter 2 to this important litoptern family, the Macraucheniidae. Micrauchenia saladensis is the first litoptern from the Bahía Inglesa Formation, Chile. The specimen includes a partial mandible, cervical and thoracic vertebrae fragments, and portions of the forelimbs (a scapula fragment, an ulna-radius fragment, seven carpals, three metapodials, two proximal phalanges and four intermediate phalanges). The postcranial anatomy of Micrauchenia saladensis is consistent with terrestrial and cursorial locomotion, which suggests an allochthonous position of this specimen within the marine Bahía Inglesa Formation. The fusion of the ulna and radius and the presence of a radial aliform expansion aligns Micrauchenia with other macraucheniines, with which it shares these features. The fusion of the ulna and radius is interpreted as a cursorial specialisation, and the aliform expansion as an adaptation for strong flexion movements and to resist higher transverse stresses during locomotion. In addition, Micrauchenia saladensis is the smallest member of the subfamily Macraucheniinae. To test the systematics and phylogenetics of this new species, previously published morphological matrices of macraucheniids were expanded by adding one dental and eight postcranial characters, and scoring Micrauchenia saladensis. I performed maximum parsimony and Bayesian phylogenetic analyses, the latter applied for the first time in a macraucheniid phylogeny. These analyses confirm Micrauchenia saladensis as a member of the subfamily Macraucheniinae, although with uncertain affinities within this subfamily. Finally, in Chapter 4 I addressed the monophyly, interfamilial relationships and timing of the familial diversification of the order Litopterna with phylogenetic methods. Based on a large collaborative matrix currently being built by the Palaeocene Mammal Working Group for exploring the affinities within Placentalia, I built a new morphological matrix with 954 dental and mandibular characters, that included the more complete and earliest members of the five well-established litoptern families: Adianthidae, Anisolambdidae, Macraucheniidae, Proterotheriidae and Sparnotheriodontidae. I also included families with controversial affinities and sometimes considered to be part of Litopterna: Protolipternidae, Indaleciidae, and Notonychopidae. The last two are often grouped as members of the order Notopterna. In addition, I included North American mioclaenids, South American kollpanines and didolodontids, and early members of the SANU orders Notoungulata, Xenungulata and Astrapotheria. I conducted maximum parsimony and undated and tip-dated Bayesian phylogenetic analyses. The obtained trees from the various analyses mostly agree showing protolipternids, didolodontids and kollpanines at the stem of a monophyletic group composed of the SANU orders, and finding Litopterna as monophyletic group composed of the families Adianthidae, Anisolambdidae, Macraucheniidae, Proterotheriidae and Sparnotheriodontidae. The trees differ in the position of the group formed by Indaleciidae and Notonychopidae, which is sometimes closely related to Litopterna and at other times closely related to Notoungulata, and also in the precise interfamilial affinities of Adianthidae and Macraucheniidae within Litopterna. The tip-dated Bayesian tree suggests that the migration from North America occurred in the earliest Palaeocene, the origin of Litopterna was in the late Palaeocene, and the migration of litopterns to Antarctica occurred in the early to middle Eocene. These results suggest that (1) didolodontids, protolipternids and kollpanines should be considered early SANUs, but not particularly closely related to any order, (2) considering the uncertainty in the exact position of the monophyletic group formed by Indaleciidae and Notonychopidae, these families should be excluded from Litopterna and potentially grouped in the order Notopterna as previously proposed, and (3) Litopterna is composed of five families (i.e., Adianthidae, Anisolambdidae, Macraucheniidae, Proterotheriidae and Sparnotheriodontidae) which form a monophyletic unit with an origin probably in the early Palaeocene. Overall, this thesis provides new insights about the tempo and mode of evolution of placental mammals through the use of cutting-edge phylogenetic methods. Crucially, this thesis as a whole represents a major step in our understanding of the anatomy and phylogenetic affinities of Darwin's enigmatic South American ungulates.