Michael O. Woodburne

The Great American Biotic Interchange: Dispersals, Tectonics, Climate, Sea Level and Holding Pens

The biotic and geologic dynamics of the Great American Biotic Interchange are reviewed and revised. Information on the Marine Isotope Stage chronology, sea level changes as well as Pliocene and Pleistocene vegetation changes in Central and northern South America add to a discussion of the role of climate in facilitating trans-isthmian exchanges. Trans-isthmian land mammal exchanges during the Pleistocene glacial intervals appear to have been promoted by the development of diverse non-tropical ecologies.

The evolution of tribospheny and the antiquity of mammalian clades

The evolution of tribosphenic molars is a key innovation in the history of Mammalia. Tribospheny allows for both shearing and grinding occlusal functions. Marsupials and placentals are advanced tribosphenic mammals (i.e., Theria) that show additional modifications of the tribosphenic dentition including loss of the distal metacristid and development of double-rank postvallum/prevallid shear. The recent discovery of Eomaia [Nature 416 (2002) 816], regarded as the oldest eutherian mammal, implies that the marsupial-placental split is at least 125 million years old. The conventional scenario for the evolution of tribosphenic and therian mammals hypothesizes that each group evolved once, in the northern hemisphere, and is based on a predominantly Laurasian fossil record. With the recent discovery of the oldest tribosphenic mammal (Ambondro) from the Mesozoic of Gondwana, Flynn et al. [Nature 401 (1999) 57] suggested that tribospheny evolved in Gondwana rather than in Laurasia. Luo et al. [Nature 409 (2001) 53; Acta Palaeontol. Pol. 47 (2002) 1] argued for independent origins of tribospheny in northern (Boreosphenida) and southern (Australosphenida) hemisphere clades, with the latter including Ambondro, ausktribosphenids, and monotremes. Here, we present cladistic evidence for a single origin of tribosphenic molars. Further, Ambondro may be a stem eutherian, making the split between marsupials and placentals at least 167 m.y. old. To test this hypothesis, we used the relaxed molecular clock approach of Thorne/Kishino with amino acid data sets for BRCA1 [J. Mammal. Evol. 8 (2001) 239] and the IGF2 receptor [Mammal. Genome 12 (2001) 513]. Point estimates for the marsupial-placental split were 182-190 million years based on BRCA1 and 185-187 million years based on the IGF2 receptor. These estimates are fully compatible with the results of our cladistic analyses.

Dispersal, Vicariance, and the Late Cretaceous to Early Tertiary Land Mammal Biogeography from South America to Australia

A review of paleontological, phyletic, geophysical, and climatic evidence leads to a new scenario of land mammal dispersal among South America, Antarctica, and Australia in the Late Cretaceous to early Tertiary epochs. New fossil land vertebrate material has been recovered from all three continents in recent years. As regards Gondwana, the present evidence suggests that monotreme mammals and ratite birds are of Mesozoic origin, based on both geochronological and phyletic grounds. The occurrence of monotremes in the early Paleocene (ca. 62 Ma) faunas of Patagonia and of ratites in late Eocene (ca. 41-37 m.y.) faunas of Seymour Island (Antarctic Peninsula) probably is an artifact of a much older and widespread Gondwana distribution prior to the Late Cretaceous Epoch. Except for South American microbiotheres being australidelphians, marsupial faunas of South America and Australia still are fundamentally disjunct. New material from Seymour Island (Microbiotheriidae) indicates the presence there of a derived taxon that resides in a group that is the sister taxon of most Australian marsupials. There is no compelling evidence that dispersal between Antarctica and Australia was as recent as ca. 41 Ma or later. In fact, the derived marsupial and placental land mammal fauna of Seymour Island shows its greatest affinity with Patagonian forms of Casamayoran age (ca. 51–54 m.y.). This suggests an earlier dispersal of more plesiomorphic marsupials from Patagonia to Australia via Antarctica, and vicariant disjunction subsequently. This is consistent with geophysical evidence that the South Tasman Rise was submerged by 64 Ma and with geological evidence that a shallow water marine barrier was present from then onward. The scenario above is consistent with molecular evidence suggesting that australidelphian bandicoots, dasyurids, and diprotodontians were distinct and present in Australia at least as early as the 63-Ma-old australidelphian microbiotheres and the ancient but not basal australidelphian,Andinodelphys, in the Tiupampa Fauna of Bolivia. Land mammal dispersal to Australia typically has been considered to be at a low level of probability (e.g., by sweepstakes dispersal). This study suggests that the marsupial colonizers of Australia included already recognizable members of the Peramelina, Dasyuromorphia, and Diprotodontia, at least, and entered via a filter route rather than by a sweepstakes dispersal.

Formation of the Isthmus of Panama

Independent evidence from rocks, fossils, and genes converge on a cohesive narrative of isthmus formation in the Pliocene. The formation of the Isthmus of Panama stands as one of the greatest natural events of the Cenozoic, driving profound biotic transformations on land and in the oceans. Some recent studies suggest that the Isthmus formed many millions of years earlier than the widely recognized age of approximately 3 million years ago (Ma), a result that if true would revolutionize our understanding of environmental, ecological, and evolutionary change across the Americas. To bring clarity to the question of when the Isthmus of Panama formed, we provide an exhaustive review and reanalysis of geological, paleontological, and molecular records. These independent lines of evidence converge upon a cohesive narrative of gradually emerging land and constricting seaways, with formation of the Isthmus of Panama sensu stricto around 2.8 Ma. The evidence used to support an older isthmus is inconclusive, and we caution against the uncritical acceptance of an isthmus before the Pliocene.

Land mammal biostratigraphy and magnetostratigraphy of the Etadunna Formation (late Oligocene) of South Australia

ABSTRACT Field work recently completed in the Lake Eyre Basin, South Australia, has resulted in the development of a land mammal (marsupial) biostratigraphy of the Etadunna Formation. Whereas traditional interpretations of the age of this sequence suggest it is about 15 m.y. old, new information indicates that the Etadunna likely is 24–26 m.y. old. In either case, it appears possible to document a four-fold fossil mammal zonation of this rock unit at lakes Palankarinna, Kanunka, Pitikanta, and Ngapakaldi, in a composite section of strata that spans at least 30 m. Magnetostratigraphic data for the same succession are generally consistent with the correlation of the Etadunna Formation sites at Lake Palankarinna with of those at lakes Kanunka, Pitikanta, and Ngapakaldi to the north, as based on paleontological information. The magnetic polarity zonation of these Etadunna Formation strata is consistent with a correlation to the world magnetic polarity time scale at about 24–26 m.y. This is the first fine-scal...

The oldest platypus and its bearing on divergence timing of the platypus and echidna clades

Monotremes have left a poor fossil record, and paleontology has been virtually mute during two decades of discussion about molecular clock estimates of the timing of divergence between the platypus and echidna clades. We describe evidence from high-resolution x-ray computed tomography indicating that Teinolophos, an Early Cretaceous fossil from Australias Flat Rocks locality (121–112.5 Ma), lies within the crown clade Monotremata, as a basal platypus. Strict molecular clock estimates of the divergence between platypus and echidnas range from 17 to 80 Ma, but Teinolophos suggests that the two monotreme clades were already distinct in the Early Cretaceous, and that their divergence may predate even the oldest strict molecular estimates by at least 50%. We generated relaxed molecular clock models using three different data sets, but only one yielded a date overlapping with the age of Teinolophos. Morphology suggests that Teinolophos is a platypus in both phylogenetic and ecological aspects, and tends to contradict the popular view of rapid Cenozoic monotreme diversification. Whereas the monotreme fossil record is still sparse and open to interpretation, the new data are consistent with much slower ecological, morphological, and taxonomic diversification rates for monotremes than in their sister taxon, the therian mammals. This alternative view of a deep geological history for monotremes suggests that rate heterogeneities may have affected mammalian evolution in such a way as to defeat strict molecular clock models and to challenge even relaxed molecular clock models when applied to mammalian history at a deep temporal scale.

The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole

Alternative hypotheses in higher–level marsupial systematics have different implications for marsupial origins, character evolution, and biogeography. Resolving the position of the South American monito del monte (Order Microbiotheria) is of particular importance in that alternate hypotheses posit sister-group relationships between microbiotheres and taxa with disparate temporal and geographic distributions: pediomyids; didelphids; dasyuromorphians; diprotodontians; all other australidelphians; and all other marsupials. Among Australasian marsupials, the placement of bandicoots is critical; competing views associate bandicoots with particular Australasian taxa (diprotodontians, dasyuromorphians) or outside of a clade that includes all other Australasian forms and microbiotheres. Affinities of the marsupial mole are also unclear. The mole is placed in its own order (Notoryctemorphia) and sister–group relationships have been postulated between it and each of the other Australasian orders. We investigated relationships among marsupial orders by using a data set that included mitochondrial and nuclear genes. Phylogenetic analyses provide support for the association of microbiotheres with Australasian marsupials and an association of the marsupial mole with dasyuromorphs. Statistical tests reject the association of diprotodontians and bandicoots together as well as the monophyly of Australasian marsupials. The origin of the paraphyletic Australasian marsupial fauna may be accounted for by (i) multiple entries of australidelphians into Australia or (ii) bidirectional dispersal of australidelphians between Antarctica and Australia.

Fossil Land Mammal from Antarctica

A fossil land mammal, apparently the first found in Antarctica, belongs to the extinct marsupial family Polydolopidae. The fossils were recovered from rocks about 40 million years old on Seymour Island, in the northern Antarctic Peninsula. The newly discovered marsupials support theories that predicted their former presence in Antarctica and strengthen proposals that Australian marsupials perhaps originated from South American species that dispersed across Antarctica when Australia still was attached to it, prior to 56 million years ago.

“South American” Marsupials from the Late Cretaceous of North America and the Origin of Marsupial Cohorts

Newly described marsupial specimens of Judithian (late Campanian) and Lancian (Maastrichtian) age in the western interior of North America (Wyoming to Alberta) have dental morphologies consistent with those expected in comparably aged sediments in South America (yet to be found). Three new Lancian species are referable to the didelphimorphian Herpetotheriidae, which suggests that the ameridelphian radiation was well under way by this time. The presence of a polydolopimorphian from Lancian deposits with a relatively plesiomorphic dental morphology and an additional polydolopimorphian taxon from Judithian deposits with a more derived molar form indicate that this lineage of typically South American marsupials was diversifying in the Late Cretaceous of North America. This study indicates that typical South American lineages (e.g. didelphimorphians and polydolopimorphians) are not the result of North American peradectian progenitors dispersing into South America at the end of the Cretaceous (Lancian), or at the beginning of the Paleocene (Puercan), and giving rise to the ameridelphian marsupials. Instead, these lineages, and predictably others as well, had their origins in North America (probably in more southerly latitudes) and then dispersed into South America by the end of the Cretaceous. Geophysical evidence concerning the connections between North and South America in the Late Cretaceous is summarized as to the potential for overland mammalian dispersal between these places at those times. Paleoclimatic reconstructions are considered, as is the dispersal history of hadrosaurine dinosaurs and boid snakes, as to their contribution to an appraisal of mammalian dispersals in the Late Cretaceous. In addition, we present a revision of the South American component of the Marsupialia. One major outcome of this process is that the Polydolopimorphia is placed as Supercohort Marsupialia incertae sedis because no characteristics currently known from this clade securely place it within one of the three named marsupial cohorts.

Climate directly influences Eocene mammal faunal dynamics in North America.

The modern effect of climate on plants and animals is well documented. Some have cautioned against assigning climate a direct role in Cenozoic land mammal faunal changes. We illustrate 3 episodes of significant mammalian reorganization in the Eocene of North America that are considered direct responses to dramatic climatic events. The first episode occurred during the Paleocene–Eocene Thermal Maximum (PETM), beginning the Eocene (55.8 Ma), and earliest Wasatchian North American Land Mammal Age (NALMA). The PETM documents a short (<170 k.y.) global temperature increase of ≈5 °C and a substantial increase in first appearances of mammals traced to climate-induced immigration. A 4-m.y. period of climatic and evolutionary stasis then ensued. The second climate episode, the late early Eocene Climatic Optimum (EECO, 53–50 Ma), is marked by a temperature increase to the highest prolonged Cenozoic ocean temperature and a similarly distinctive continental interior mean annual temperature (MAT) of 23 °C. This MAT increase [and of mean annual precipitation (MAP) to 150 cm/y) promoted a major increase in floral diversity and habitat complexity under temporally unique, moist, paratropical conditions. Subsequent climatic deterioration in a third interval, from 50 to 47 Ma, resulted in major faunal diversity loss at both continental and local scales. In this Bridgerian Crash, relative abundance shifted from very diverse, evenly represented, communities to those dominated by the condylarth Hyopsodus. Rather than being “optimum,” the EECO began the greatest episode of faunal turnover of the first 15 m.y. of the Cenozoic.