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Summarized results from the retroposon study by Dodt et al. (2017) and the genomic phylogeny of Nilsson et al. (2017) showing supporting (red circles) and conflicting (black circles) retroposons, and mximum likelihood bootstrap support, respectively. Photographs show (from the top) Macropus giganteus, Osphranter rufus, Wallabia bicolor and Notamacropus rufogriseus Photograph credits: C. Fruciano, M. Celik and M. Phillips.
Source publication
Kangaroos and wallabies of the Macropus complex include the largest extant marsupials and hopping mammals. They have traditionally been divided among the genus Macropus (with three subgenera: Macropus, Osphranter and Notamacropus) and the monotypic swamp wallaby, Wallabia bicolor. Recent retrotransposon and genome-scale phylogenetic analyses clarif...
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... is now confirmed with retrotransposons (Dodt et al., 2017) and genome-scale sequence analysis ) that Wallabia and Notamacropus form a wallaby clade, with the larger wallaroos and kangaroos of Osphranter and Macropus confidently placed as consecutive outgroups (Fig. 1). Nevertheless, the retrotransposons and genome fragments reveal substantial incomplete lineage sorting and probably introgression between Wallabia, Osphranter, Macropus, Notamacropus and an extinct 'Macropus' stem taxon. This could explain much of the previous incongruence between loci (see Phillips et al., 2013). Incidences of deep ...
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... partitioned the nuclear data by gene, following Meredith et al. (2008) or following a PartitionFinder2 (Lanfear et al., 2016) scheme that also separates third codon positions from combined first and second codon positions for BRCA1 and IRBP (Supporting Information, Tables S4, S5). The same topology is reconstructed under both schemes, along with near-identical bootstrap support (see Supporting Information, Fig. S1). For mtDNA, the RNA genes were partitioned into stem and loop sites following Phillips et al. (2013), and the protein-coding sequences were partitioned by codon position. ...
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... Bayesian (MrBayes) and ML (IQ-TREE) analyses of the DNA dataset comprising five nuclear and four mitochondrial genes are consistent with the relationships between subgenera that have emerged with overwhelming support from retrotransposon and genome-scale sequence studies (Fig. 1). As shown in Figure 2, Wallabia is sister to Notamacropus, with Osphranter and Macropus diverging successively deeper. There is moderately strong support for Macropodini (81% maximum likelihood bootstrap probability (ML-BP), 0.97 Bayesian posterior probability (BPP)), which in addition to 'Macropus', includes Lagorchestes, Setonix and ...
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... indices and standard deviation for traditional Macropus (including Macropus, Notamacropus and Osphranter), Petrogale and Notamacropus with and without allometric correction. Figure S1. Phylogenetic relationships of the Macropodiformes inferred from five nuclear and four mitochondrial sequences (10.35 kb). ...
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... reduces the influence of high saturation inherent in the rapidly evolving control region sequences and allows direct comparison with the tree in Figure 3. Nodes were set as follows: A, 'Macropus' normal (6.57, 0.1); B, Osphranter-Notamacropus normal (6.07, 0.1); C, Osphranter, normal (4.74, 0.1); D, core-Notamacropus, normal (4.615, 0.1); E, Macropus, normal (2.30, 0.1); F, wallaroos, normal (3.64, 0.1); and G, Osphranter antilopinusOsphranter robustus, normal (2.045, 0.1). Figure S8. Scatterplot of scores along principal components 3 and 4 for the 'Macropus' dataset containing allometric variation (A) and removing allometric variation (B) Figure S10. Unconstrained minimum evolution tree based on cranial morphometric distances not corrected for allometry. ...
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... minimum evolution tree based on cranial morphometric distances not corrected for allometry. Figure S11. Minimum evolution phylogeny based on cranial morphometric distances corrected for allometry. ...
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... evolution phylogeny based on cranial morphometric distances corrected for allometry. Figure S12. Topology (based on the molecular phylogeny) used to constrain minimum evolution analyses on cranial morphometric distances. ...
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... (based on the molecular phylogeny) used to constrain minimum evolution analyses on cranial morphometric distances. Figure S13. Minimum evolution tree based on cranial morphometric distances not corrected for allometry and constrained according to the molecular tree. ...
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... clade stems with branch lengths greater than zero are represented in red. Figure S14. Minimum evolution tree based on cranial morphometric distances corrected for allometry and constrained according to the molecular tree. ...
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... clade stems with branch lengths greater than zero are represented in red. Figure S15. Minimum evolution phylogeny on cranial morphometric distances not corrected for allometry, and with landmarks 9 and 31 (which have been estimated in Macropus greyi) excluded from analysis. ...
Citations
... The difference between species-means and phylogenetically-corrected species-means indicates that there is variation between species, but this is more apparent when examining the intraspecific scaling of separate species. Within the Macropus species complex (see Celik et al. (2019) There are no reports that have both body mass and calcaneus length for individuals, however species-mean length shows strong positive allometry (species-means: ∝ M 0.406 ± 0.041 , corrected species-means: ∝ M 0.392 ± 0.058 ). Calcaneus length is approximately equal to the moment arm, r, the distance from the gastrocnemius and plantaris muscle line of action to the ankle joint centre of rotation. ...
... Red colours indicate little sampling while blue colours indicate extensive sampling. In some studies, Macropus has been sub-divided into separate genera or subgenera: Macropus, Osphranter, and Notamacropus(Celik et al. 2019;Meredith et al. 2009)). ...
Macropods such as kangaroos look and move unlike any other animal. These two characteristics are tightly linked, but they are often studied independently. This thesis uses morphologically-informed musculoskeletal models to evaluate both experimental and novel simulated hopping locomotion. It mechanistically links the underlying morphology to the limits of speed and energetic performance, which is of particular interest in macropods because metabolic cost of locomotion is uniquely independent of speed.
The first chapter is a meta-analysis of the phylogenetic scaling of skeletal, muscle and tendon morphology within Macropodoidea (kangaroos, wallabies and potoroos), as well as a review of hopping locomotion, including gait parameters and performance. The review identified knowledge gaps where experimental methods reached their limits; these questions, in particular, would benefit from a new modelling approach.
The second chapter explored why speed-independent metabolic cost is unique to macropods larger than 3 kg, given that the two largest likely contributions to cost or cost savings (high strain tendons and features of the hopping gait) are found among various other taxa. To do this, I constructed an OpenSim musculoskeletal model of a grey kangaroo. I used the model to analyse empirical kinetic and kinematic data, in the process uncovering a change in hindlimb posture that could disproportionately increase elastic strain energy storage with speed, and thereby contribute to constant metabolic cost for the slow hopping speeds that were measured. Macropods have a unique combination of adaptable posture and appropriate tendon morphology, which may explain why constant cost is unique to these species.
Kangaroo metabolic cost has been predicted to increase with stride frequency, but the natural increase in stride frequency would occur at speeds faster than those for which their oxygen consumption has been successfully measured. The third chapter developed the musculoskeletal model to operate within a predictive simulation framework to achieve faster speeds. I found that the cost remains linear, challenging the prediction that metabolic cost is constant at low speeds due to constant stride frequency. The simulation results were verified against the dataset compiled in the meta-analysis, which was independent of the model inputs, and to the empirical kinetic and kinematic data analysed in chapter two, for the range of speeds and sizes that overlapped.
The fourth chapter arose from the morphological portion of the review. Previous scaling studies identified Achilles tendon stress as the predominant limit on kangaroo maximum speed and maximum body mass because the tendons were projected to fail at approximately 150 kg. However, previous research was unable to consider gait parameters for possible avenues of stress reduction, as such large kangaroos are now extinct. By geometrically scaling the model, I discovered that tendon stress did not prevent hopping as the expected increase in force was distributed over longer ground contact durations. Tendon stress increasingly limited maximum speed at greater masses, but the more pressing scaling problem for giant kangaroos was muscle strength. Additionally, giant kangaroos, unlike other species, may not benefit from lower mass-specific metabolic costs as they increase in size. Consequently, their comparative energetic performance declined. This likely leads to a maximum viable size for economical hopping.
... An alternative approach to character-based methods for reconstructing phylogeny from GMM data is to create trees based on distances (i.e., Procrustes, Euclidean) between taxa using cluster analysis. For example, neighbour-joining [NJ; 53] [e.g., 23,24,35,44,[54][55][56] and unweighted pair group method with arithmetic mean [UPGMA; 58] [e.g., 24,35,44,56,57,59,60] or other methods such as minimum evolution [ME; 61] [e.g., 59] and maximum likelihood using flexibly weighted least squares methods [fWLS; e.g., 62,63]. ...
Background
Isolating phylogenetic signal from morphological data is crucial for accurately merging fossils into the tree of life and for calibrating molecular dating. However, subjective character definition is a major limitation which can introduce biases that mislead phylogenetic inferences and divergence time estimation. The use of quantitative data, e.g., geometric morphometric (GMM; shape) data can allow for more objective integration of morphological data into phylogenetic inference. This systematic review describes the current state of the field in using continuous morphometric data (e.g., GMM data) for phylogenetic reconstruction and assesses the efficacy of these data compared to discrete characters using the PRISMA-EcoEvo v1.0. reporting guideline, and offers some pathways for approaching this task with GMM data. A comprehensive search string yielded 11,123 phylogenetic studies published in English up to Oct 2023 in the Web of Science database. Title and abstract screening removed 10,975 articles, and full-text screening was performed for 132 articles. Of these, a total of twelve articles met final inclusion criteria and were used for downstream analyses.
Results
Phylogenetic performance was compared between approaches that employed continuous morphometric and discrete morphological data. Overall, the reconstructed phylogenies did not show increased resolution or accuracy (i.e., benchmarked against molecular phylogenies) as continuous data alone or combined with discrete morphological datasets.
Conclusions
An exhaustive search of the literature for existing empirical continuous data resulted in a total of twelve articles for final inclusion following title/abstract, and full-text screening. Our study was performed under a rigorous framework for systematic reviews, which showed that the lack of available comparisons between discrete and continuous data hinders our understanding of the performance of continuous data. Our study demonstrates the problem surrounding the efficacy of continuous data as remaining relatively intractable despite an exhaustive search, due in part to the difficulty in obtaining relevant comparisons from the literature. Thus, we implore researchers to address this issue with studies that collect discrete and continuous data sets with directly comparable properties (i.e., describing shape, or size).
Supplementary Information
The online version contains supplementary material available at 10.1186/s12862-024-02313-3.
... Osphranter rufus was created from a composite of images in the public domain; Sthenurus stirlingi was modified from Regal in Janis et al. (2014), with permission from Brian Regal; Dendrolagus goodfellowi was created from a photo taken by BJ of an animal in the Bristol Zoological Gardens; Protemnodon anak was created from a photo taken by CMJ of the mounted specimen in the South Australian Museum. The genera grouped together here of Macropus, Osphranter and Notamacropus, previously all included within Macropus, are known as the "Macropus complex" (Celik et al. 2019); their interrelationships remain in debate. Figure created in Adobe Illustrator by Science Graphic Design (www. ...
Kangaroos (Macropodoidea) display a diversity of locomotor modes, from bounding quadrupedally to hopping bipedally; but hopping has a body mass limit, which was exceeded by a number of extinct taxa. In the Pleistocene, a variety of “giant” kangaroos existed, both within the extinct subfamily Sthenurinae and the extant subfamily Macropodinae (both within the family Macropodidae). Sthenurines have been previously considered to have a type of locomotion (bipedal striding) different from extant kangaroos, but the primary locomotor mode of the large species of the extinct “giant” macropodine genus Protemnodon, closely related to extant large kangaroos, has undergone little question and has been assumed to be hopping. Here, the association between limb proportions and locomotor mode across Macropodoidea is assessed by examination of functional limb indices. We show that large (> 100 kg) Protemnodon species are unlike any other known macropodoids; their position in this functional morphospace, along with previously published evidence on humeral morphology, supports a prior hypothesis of a primarily quadrupedal mode of locomotion, likely some sort of bounding.
... marsupials) has been demonstrated for Solanum species in arid Australia (Symon 1986). However, the origins and diversification of several of these spinescent clades in Cryptandra (e.g. C. multispina, C. micrantha) pre-date the origins of extant marsupial browsers in Australia (post-10 Myr; Celik et al. 2019). Thus, spinescence may have arisen in these lineages in response to non-marsupial (e.g. ...
The Australian continent has experienced progressive aridification since the Miocene, spurring recent radiations of arid-adapted lineages and the likely decline of mesic biotic groups. While examples of the former have been relatively well-documented, post-Miocene declines of non-arid sclerophyllous floras are less well understood. Here, we present a well-sampled time-calibrated nuclear phylogeny (140 accessions representing 60/65 species) of an Australian plant genus (Cryptandra Sm.: Rhamnaceae) and using ancestral range reconstructions and diversification analyses, elucidate its evolutionary history through space and time. We used high-throughput sequencing to recover 30 orthologous nuclear loci and BioGeoBEARS to infer ancestral areas. We show that the present-day distribution of Cryptandra can be explained by multiple vicariance events followed by in situ diversification with little exchange between regions. All diversification models show a speciation rate decline in Cryptandra after its radiation in the Miocene (c. 23 Mya). This coincides with aridification episodes across Australia and indicates that diversification of this genus has been negatively affected by the expansion of aridity. We also show that there were no significant differences in diversification rates between spinescent and non-spinescent Cryptandra lineages, suggesting that spinescent lineages may be the legacies of selection from extinct megaherbivores.
... Species designations are those provided by the institutions holding the specimens unless there are revisionary changes that are simply nomenclatural. In the case of specimens previously assigned to Macropus eugenii and M. robustus, we follow Celik et al. (2019) in assigning them, respectively, to Notamacropus eugenii and Osphranter robustus. The older literature consulted for this study does not generally provide sufficient information to allow revision of species-level nomenclature, and for the most part the names used in those papers concerned have been retained. ...
... The current study examined the developmental pattern of the ethmoid and turbinal elements in a different species of marsupial mammal that is outside the clade of Didelphidae. We examined a growth series of pouch young of the species Notamacropus eugenii (formerly Macropus eugenii, see [18]), the tammar wallaby, which belongs to the clade Macropodidae. The ethmoid of an adult N. eugenii was studied from imaging of a skull via high-resolution X-ray computed tomography (CT). ...
... Notamacropus eugenii, the tammar wallaby, was previously known as Macropus eugenii, but the taxonomy for this species was recently revised based on retrotransposon and genome-scale phylogenetic analyses [18]. Notamacropus eugenii is a small wallaby with a body size of 4-7 kg and is known from southwestern Western Australia, southern South Australia and multiple nearby islands [19,20]. ...
The homologies of the turbinals (scroll bones) of the ethmoid are not well understood, including the potential implication for understanding mammalian phylogeny. Here we examine the postnatal development of this anatomical system in a marsupial mammal because previous work has shown that the adult pattern of five endoturbinals (ethmoturbinals) and two ectoturbinals (frontoturbinals) is conserved. Furthermore, marsupial phylogeny is fairly well resolved and provides a solid evolutionary framework for examining turbinal homologies. In this study, we documented the development of the ethmoid of the tammar wallaby, Notamacropus eugenii , using histology and computed tomography imagery of a growth series of pouch young. The pattern of development of the turbinal elements in the wallaby was compared to that in didelphids, as described in previous work. We found that four ethmoturbinals initially develop, followed later in development by an interturbinal; these five elements then develop into the bony endoturbinals found in adults. These data support the idea that endoturbinal III, derived from an interturbinal, has a distinctive development pattern from the other endoturbinals. This is consistent with what is seen in the didelphid marsupials, Caluromys philander and Monodelphis domestica , suggesting this is a common developmental pattern for marsupials.
This article is part of the theme issue ‘The mammalian skull: development, structure and function’.
... Kangaroos belong to the Diprotodontia order and are members of the Macropodidae family. 1 Macropodidae include a diverse group of > 60 extant species of marsupials native to various habitats (rainforests, woodlands, grasslands, rocky cliffs, and deserts) in Australia and New Guinea. A total of 63 Macropodidae species are listed on the International Union for Conservation of Nature (IUCN) Red List, of which four are extinct, three are critically endangered, eight are endangered, 14 are vulnerable and 10 are near threatened. 2 Wild macropods face challenges of urbanization, road deaths, drought, disease, and wildfires. ...
The purpose of this prospective and anatomic study was to describe the ultrasonographic anatomy of the kidneys, urinary bladder, adrenal glands, spleen, liver, gall bladder, and gastrointestinal tract in healthy juvenile eastern grey kangaroos (Macropus giganteus). As ultrasonographic descriptions are lacking in marsupial species, it was also conducted to develop a systematic approach for abdominal ultrasonographic evaluation in the kangaroo and to provide preliminary quantitative and qualitative references. Ten macropod cadavers (eight eastern grey kangaroos and two swamp wallabies (Wallabia bicolor)) were used for initial dissections and preliminary ultrasonographic examinations. Seven eastern grey kangaroos (four females and three males; mean mass 18 kg (±4.5)) were ultrasonographically examined under heavy sedation in lateral recumbency. The gaseous forestomach occupied a large proportion of the entire abdomen ultrasonographically; therefore, the majority of cranial landmarks were based on an intercostal approach comparable to a deep-chested dog. Compared to domestic species, ultrasonographic differences in anatomy include the forestomach, hindstomach, liver orientation, distinguishable adrenal glands, splenic branching, and epipubic bones, all of which were described. The study was limited by the small sample size (7) and weight range (14-25 kg). The systematic approach and description of the normal ultrasonographic anatomy of the abdominal organs in the eastern grey kangaroo should provide a foundation for the ultrasonographic diagnosis and interpretation of abdominal disease in this species.
... Sicista betulina (Pallas, 1779) Gambaryan et al. (1980) Canis familiaris Linnaeus, 1758 Davis (1955) (see Davis, 1964;Turnbull, 1970) Table 1). We followed Celik et al. (2019) for kangaroo and wallaby taxonomic nomenclature. ...
Masticatory muscle features allow for an understanding of how dietary habits and masticatory functions have evolved across mammalian lineages. Herbivorous mammals were traditionally classified as pertaining to either ‘ungulate-grinding’ or ‘rodent-gnawing’ morphotypes, but those classes might not adequately encompass the diversity of past and present herbivores. We compiled data for 104 herbivorous (nine orders, including new data for 31 species) and ten non-herbivorous (five orders) extant species and for four extinct taxa, in order to construct a more comprehensive scheme of masticatory morphotypes. A myological phylomorphospace revealed 15 morphotypes, which were tested statistically and interpreted morphofunctionally. Extant herbivorous morphotypes diversified along two main pathways that did not reflect the traditional types. Additionally, some extinct herbivores adapted along alternative pathways to those of extant forms. Early mammaliaforms and mammals possessed muscle proportions almost identical to those of living carnivores. Several more plesiomorphic herbivorous morphotypes were recognized, with some of them retaining generalized myological proportions. The rodent disparity was remarkable and could not be encompassed by a single category or pathway. Features of some derived euungulates and diprotodonts resembled rodents, but only a few extinct euungulates and extant wombats converged closely with them. Criteria for selecting models for palaeobiological reconstructions are discussed.
... These shape-based methods are increasingly being considered for phylogenetic inference (e.g., Parins-Fukuchi 2018, Ascarrunz et al. 2019), because the subjectivity of character choice and state assignments are obviated, although landmarking is still required in most instances. A nice property of geometric morphometrics is that correlates of size (or allometry) can be readily excluded, regressing shape against centroid size, as Celik et al. (2019) did for inferring macropod phylogeny. In principle, regressions against shape could also be used to remove covariation with ecological or other life history traits, with the expectation that the residuals contain higher fidelity phylogenetic signals. ...
Large-scale molecular datasets have generally outperformed morphological data for inferring phylogeny, and sources of error in the latter are poorly understood. The morphologically and ecologically diverse marsupial order Diprotodontia (kangaroos and their relatives, the koala, wombats and possums) is well suited to considering these issues. Recent molecular results provide a phylogenetic benchmark for comparing previous molecular and morphological studies, encompassing all of the major phylogenetic data sources and methods that have been employed over the past 50 years. We show here that most molecular methodologies and ‘informal-comparative’ morphological studies have inferred diprotodontian relationships that closely resemble the recent molecular consensus. However, and perhaps surprisingly, algorithmic morphology, such as maximum parsimony analysis of morphological matrices, has inferred markedly inaccurate phylogenies, and is not improved by re-analysis with more recently developed, model-based (e.g., likelihood and Bayesian) methods. This is particularly concerning because algorithmic morphology is the primary approach for integrating fossils into the tree of life, and hence, for both calibrating molecular timescales and extending phylogenetic inferences of evolutionary processes beyond the snapshot provided by modern species. A novel simulation study presented here suggests that the inaccuracies in the marsupial algorithmic morphology studies partly stem from functional and body-size correlations among taxa that over-ride phylogenetic signals. We use the results to trial a reverse engineered phylogeny approach to correcting for such functional and developmental correlations among morphological data. In addition, we interrogated a newly published, densely taxon-sampled morphological matrix. Deeper level phylogeny reconstruction was improved by including fossils alongside extant taxa and counterintuitively, by increased effort to resolve relationships among shallow taxa.
Matthew J. Phillips [m9.phillips@qut.edu.au]; Mélina A. Celik [melina.celik@gmail.com] School of Biology and Environmental Science, Queensland University of Technology, 2 George Street, Brisbane, Qld, 4000, Australia; Robin M.D Beck [r.m.d.beck@salford.ac.uk] Ecosystems and Environment Research Centre, School of Science, Engineering and Environment, University of Salford, Manchester, UK.
... Fresh adult male specimens from the south-eastern part of the range of the kultarr are required to resolve this matter. The two species of the newly defined Antechinomys form a distinct monophyletic lineage within Sminthopsini, supporting their generic distinction from both Ningaui and Sminthopsis, as suggested by Celik et al. (2019) for the distinction of Wallabia from Notamacropus. ...
Morphological and molecular studies have consistently suggested that Sminthopsis, as currently defined, is rendered paraphyletic by the kultarr (Antechinomys laniger). They have also suggested a sister relationship between the kultarr and the long-tailed dunnart. Based on DNA sequence data from multiple mitochondrial and nuclear gene loci we reassign the long-tailed dunnart (formerly Sminthopsis longicaudata) to Antechinomys. Although there is good evidence of genetic structure within the kultarr (A. laniger), it does not correspond to the two currently recognised subspecies, viz A. laniger laniger and A. l. spenceri. We conclude that Antechinomys consists of two species, A. laniger and A. longicaudatus, consistent with morphology. We suggest that the observed genetic and morphological variation within A. laniger merits a more thorough investigation of more samples from across its range to resolve the taxonomy.
