The marsupial lion, Thylacoleo carnifex, was the largest-ever marsupial carnivore, and is one of the most iconic extinct Australian vertebrates. With a highly-specialised dentition, powerful forelimbs and a robust build, its overall morphology is not approached by any other mammal. However, despite >150 years of attention, fundamental aspects of its biology remain unresolved. Here we analyse an assemblage of claw marks preserved on surfaces in a cave and deduce that they were generated by marsupial lions. The distribution and skewed size range of claw marks within the cave elucidate two key aspects of marsupial lion biology: they were excellent climbers and reared young in caves. Scrutiny of >10,000 co-located Pleistocene bones reveals few if any marsupial lion tooth marks, which dovetails with the morphology-based interpretation of the species as a flesh specialist.
Sthenurine kangaroos (Marsupialia, Diprotodontia, Macropodoidea) were an extinct subfamily within the family Macropodidae (kangaroos and rat-kangaroos). These “short-faced browsers” first appeared in the middle Miocene, and radiated in the Plio-Pleistocene into a diversity of mostly large-bodied forms, more robust than extant forms in their build. The largest (Procoptodon goliah) had an estimated body mass of 240 kg, almost three times the size of the largest living kangaroos, and there is speculation whether a kangaroo of this size would be biomechanically capable of hopping locomotion. Previously described aspects of sthenurine anatomy (specialized forelimbs, rigid lumbar spine) would limit their ability to perform the characteristic kangaroo pentapedal walking (using the tail as a fifth limb), an essential gait at slower speeds as slow hopping is energetically unfeasible. Analysis of limb bone measurements of sthenurines in comparison with extant macropodoids shows a number of anatomical differences, especially in the large species. The scaling of long bone robusticity indicates that sthenurines are following the “normal” allometric trend for macropodoids, while the large extant kangaroos are relatively gracile. Other morphological differences are indicative of adaptations for a novel type of locomotor behavior in sthenurines: they lacked many specialized features for rapid hopping, and they also had anatomy indicative of supporting their body with an upright trunk (e.g., dorsally tipped ischiae), and of supporting their weight on one leg at a time (e.g., larger hips and knees, stabilized ankle joint). We propose that sthenurines adopted a bipedal striding gait (a gait occasionally observed in extant tree-kangaroos): in the smaller and earlier forms, this gait may have been employed as an alternative to pentapedal locomotion at slower speeds, while in the larger Pleistocene forms this gait may have enabled them to evolve to body sizes where hopping was no longer a feasible form of more rapid locomotion.
The Tasmanian tiger or thylacine (Thylacinus cynocephalus) was the largest carnivorous Australian marsupial to survive into the modern era. Despite last sharing a common ancestor with the eutherian canids ~160 million years ago, their phenotypic resemblance is considered the most striking example of convergent evolution in mammals. The last known thylacine died in captivity in 1936 and many aspects of the evolutionary history of this unique marsupial apex predator remain unknown. Here we have sequenced the genome of a preserved thylacine pouch young specimen to clarify the phylogenetic position of the thylacine within the carnivorous marsupials, reconstruct its historical demography and examine the genetic basis of its convergence with canids. Retroposon insertion patterns placed the thylacine as the basal lineage in Dasyuromorphia and suggest incomplete lineage sorting in early dasyuromorphs. Demographic analysis indicated a long-term decline in genetic diversity starting well before the arrival of humans in Australia. In spite of their extraordinary phenotypic convergence, comparative genomic analyses demonstrated that amino acid homoplasies between the thylacine and canids are largely consistent with neutral evolution. Furthermore, the genes and pathways targeted by positive selection differ markedly between these species. Together, these findings support models of adaptive convergence driven primarily by cis-regulatory evolution.
Recent studies have demonstrated a close resemblance between some handedness patterns in great apes and humans [1-3]. Despite this, comparative systematic investigations of manual lateralization in non-primate mammals are very limited [4, 5]. Among mammals, robust population-level handedness is still considered to be a distinctive human trait [6, 7]. Nevertheless, the comprehensive understanding of handedness evolution in mammals cannot be achieved without considering the other large mammalian lineage, marsupials. This study was designed to investigate manual lateralization in non-primate mammals using the methodological approach applied in primate studies. Here we show that bipedal macropod marsupials display left-forelimb preference at the population level in a variety of behaviors in the wild. In eastern gray and red kangaroos, we found consistent manual lateralization across multiple behaviors. This result challenges the notion that in mammals the emergence of strong “true” handedness is a unique feature of primate evolution. The robust lateralization in bipedal marsupials stands in contrast to the relatively weak forelimb preferences in marsupial quadrupeds, emphasizing the role of postural characteristics in the evolution of manual lateralization as previously suggested for primates [8-10]. Comparison of forelimb preferences in seven marsupial species leads to the conclusion that the interspecies differences in manual lateralization cannot be explained by phylogenetic relations, but rather are shaped by ecological adaptations. Species' postural characteristics, especially bipedality, are argued to be instrumental in the origin of handedness in mammals.
Free range exhibits are becoming increasingly popular in zoos as a means to enhance interaction between visitors and animals. However very little research exists on the impacts of visitors on animal behaviour and stress in free range exhibits. We investigated the effects of visitor number on the behaviour and stress physiology of Kangaroo Island (KI) Kangaroos, Macropus fuliginosus fuliginosus, and Red Kangaroos, Macropus rufus, housed in two free range exhibits in Australian zoos. Behavioural observations were conducted on individual kangaroos at each site using instantaneous scan sampling to record activity (e.g., vigilance, foraging, resting) and distance from the visitor pathway. Individually identifiable faecal samples were collected at the end of each study day and analysed for faecal glucocorticoid metabolite (FGM) concentration. When visitor number increased, both KI Kangaroos and Red Kangaroos increased the time spent engaged in visitor-directed vigilance and KI Kangaroos also increased the time spent engaged in locomotion and decreased the time spent resting. There was no effect of visitor number on the distance kangaroos positioned themselves from the visitor pathway or FGM concentration in either species. While there are limitations in interpreting these results in terms of fear of visitors, there was no evidence of adverse effects animal welfare in these study groups based on avoidance behaviour or stress physiology under the range of visitor numbers that we studied. Zoo Biol. XX:XX-XX, 2015. © 2015 Wiley Periodicals, Inc.
Fundamental differences in methane (CH4) production between macropods (kangaroos) and ruminants have been suggested and linked to differences in the composition of the forestomach microbiome. Using six western grey kangaroos (Macropus fuliginosus) and four red kangaroos (Macropus rufus), we measured daily absolute CH4 production in vivo as well as CH4 yield (CH4 per unit of intake of dry matter, gross energy or digestible fibre) by open-circuit respirometry. Two food intake levels were tested using a chopped lucerne hay (alfalfa) diet. Body mass-specific absolute CH4 production resembled values previously reported in wallabies and non-ruminant herbivores such as horses, and did not differ with food intake level, although there was no concomitant proportionate decrease in fibre digestibility with higher food intake. In contrast, CH4 yield decreased with increasing intake, and was intermediate between values reported for ruminants and non-ruminant herbivores. These results correspond to those in ruminants and other non-ruminant species where increased intake (and hence a shorter digesta retention in the gut) leads to a lower CH4 yield. We hypothesize that rather than harbouring a fundamentally different microbiome in their foregut, the microbiome of macropods is in a particular metabolic state more tuned towards growth (i.e. biomass production) rather than CH4 production. This is due to the short digesta retention time in macropods and the known distinct ‘digesta washing’ in the gut of macropods, where fluids move faster than particles and hence most likely wash out microbes from the forestomach. Although our data suggest that kangaroos only produce about 27% of the body mass-specific volume of CH4 of ruminants, it remains to be modelled with species-specific growth rates and production conditions whether or not significantly lower CH4 amounts are emitted per kg of meat in kangaroo than in beef or mutton production.
Adoption is rare in animals and is usually attributed to kin selection. In a 6-year study of eastern grey kangaroos (Macropus giganteus), 11 of 326 juveniles were adopted. We detected eight adoptions by observing behavioural associations and nursing between marked mothers and young and three more by analysing the relatedness of mothers and young using microsatellite DNA. Four adoptions involved reciprocal switches and three were by mothers whose own pouch young were known to subsequently disappear. Adoptive mothers were not closely related to each other or to adoptees but adoptive mothers and young associated as closely as did biological pairs, as measured by half-weight indices. Switch mothers did not associate closely. Maternal age and body condition did not influence the likelihood of adoption but females were more likely to adopt in years with high densities of females with large pouch young. Adoption did not improve juvenile survival. We conclude that adoptions in this wild population were potentially costly and likely caused by misdirected care, suggesting that eastern grey kangaroos may have poorly developed mother-offspring recognition mechanisms.
Phylogeographic studies around the world have identified refugia where fauna were able to persist during unsuitable climatic periods, particularly during times of glaciation. In Australia the effects of Pleistocene climate oscillations on rainforest taxa have been well studied but less is known about the effects on mesic-habitat fauna, such as the eastern grey kangaroo (Macropus giganteus). The eastern grey kangaroo is a large mammal that is common and widespread throughout eastern Australia, preferring dry mesic habitat, rather than rainforest. As pollen evidence suggests that the central-eastern part of Australia (southeast Queensland and northern New South Wales) experienced cycles of expansion in mesic habitat with contraction in rainforests, and vice versa during glacial and interglacial periods, respectively, we hypothesise that the distribution of the eastern grey kangaroo was affected by these climate oscillations and may have contracted to mesic habitat refugia. From 375 mitochondrial DNA control region sequences from across the distribution of eastern grey kangaroos we obtained 108 unique haplotypes. Phylogenetic analysis identified two clades in Queensland, one of which is newly identified and restricted to a small coastal region in southern Queensland north of Brisbane, known as the Sunshine Coast. The relatively limited geographic range of this genetically isolated clade suggests the possibility of a mesic habitat refugium forming during rainforest expansion during wetter climate cycles. Other potential, although less likely, reasons for the genetic isolation of the highly distinct clade include geographic barriers, separate northward expansions, and strong local adaptation.
When moving slowly, kangaroos plant their tail on the ground in sequence with their front and hind legs. To determine the tail’s role in this ‘pentapedal’ gait, we measured the forces the tail exerts on the ground and calculated the mechanical power it generates. We found that the tail is responsible for as much propulsive force as the front and hind legs combined. It also generates almost exclusively positive mechanical power, performing as much mass-specific mechanical work as does a human leg during walking at the same speed. Kangaroos use their muscular tail to support, propel and power their pentapedal gait just like a leg.
Parental care in animal evolution has long fascinated biologists, but tracing this complex of behavioural repertoires is challenging, as these transitory states often leave no corporeal traces as fossils. Among modern invertebrates, the tanaidaceans (Malacostraca: Peracarida), a lineage of marsupial crustaceans, show an interesting variety of brooding strategies. Here we report on fossil tanaidaceans from the Cretaceous of Spain and France that provide conclusive evidence for marsupial care of brood-offspring. Two exceptionally preserved female specimens of Alavatanais carabe and A. margulisae from Late Albian Peñacerrada I amber (Spain) possess four pairs of rudimentary oostegites, indicating formation of a marsupium. From Recent data, given the taxonomic distribution of a marsupium of four pairs of oostegites, we hypothesize that this may be plesiomorphic for the Tanaidomorpha. We also report on a peculiar tanaidacean specimen referable to the fossil family Alavatanaidae, Daenerytanais maieuticus gen. et sp. nov., from Early Cenomanian La Buzinie amber (France), preserved with its marsupial pouch and content. Our discoveries provide early evidence of the peracarid reproductive strategy, as seen in modern Tanaidacea, and argue that this form of parental care may have played a role in the diversification of the lineage during this period.