Paleobiology of Argyrolagus (Marsupialia, Argyrolagidae): an astonishing case of bipedalism among South American mammals

Abstract

Argyrolagus constitutes, both for its craniodental and postcranial anatomy, one of the most notably specialized South American Neogene metatherians. Differentiating it from any other South American mammal, bipedal jumping has been proposed for Argyrolagus, even though this hypothesis was not supported by morphofunctional studies. Here, we describe the postcranium of A. scaglai (from the Pliocene of Argentina), perform a functional analysis, and interpret it against a varied background of locomotor adaptations of extant mammals. The configuration of joints, the degree of development and location of muscular insertions were mainly analyzed, and functional indices were evaluated. This study indicates that Argyrolagus had stabilized glenohumeral and humeroulnar joints, a great development of the arm retractors, flexors-extensors of the digits, pronator, and supinator muscles, low restrictive humeroradial joint, powerful extensor muscles of the hip, knee, and ankle, good development of the iliac muscle, and restrictive hind limb joints. Joint configurations are interpreted to be optimal to resist the impacts during jumping, avoiding dislocation, compatible with digging activity. A compromise between the capacities to dig and manipulate objects is inferred. It is concluded that Argyrolagus had bipedal jumping locomotion as well as good capacity to dig, constituting an astonishing case of convergence with the small bipedal rodents and small Australian macropodids. We suggest that bipedal jumping in Miocene and Pliocene argyrolagids should not be necessarily related to a particular arid environment. Finally, we evaluate the importance of postcranial features to understand the phylogenetic relationships of Argyrolagidae in a comprehensive phylogeny of Metatheria.

Craniodental morphology and phylogeny of marsupials

“…We also constrained †Herpetotherium (the relationship of which to Marsupialia is unresolved in our morphological and undated total-evidence analyses; see figs. [30][31][32] to fall outside Marsupialia, in agreement with the majority of published phylogenetic analyses (Beck et al, 2008a;Horovitz et al, 2008;Horovitz et al, 2009;Beck et al, 2014;Forasiepi et al, 2014a;Suarez et al, 2015;Beck et al, 2016;Lorente et al, 2016;Carneiro and Oliveira, 2017b;Carneiro and Oliveira, 2017a;Maga and Beck, 2017;Carneiro, 2018;Carneiro et al, 2018;Engelman et al, 2018;Muizon et al, 2018;Abello and Candela, 2019;Carneiro, 2019;Rangel et al, 2019;Ladevèze et al, 2020;Muizon and Ladevèze, 2020). A full justification for constraining and calibrating these and other nodes is given in Appendix 3.…”

“…Instead, we acknowledge that retroposon insertion studies (Nilsson et al, 2010;Gallus et al, 2015) and phylogenomic analyses (Duchene et al, 2018) collectively provide strong evidence that Microbiotheria, in fact, falls outside a clade comprising the four modern Australian orders (Eomarsupialia sensu Beck et al, 2014). Similarly, although our morphological and totalevidence analyses consistently placed †Yalkaparidon with Paucituberculata, we do not diagnose this clade below, because the position of †Yalkaparidon has varied considerably in other published studies (Beck et al, 2014;Beck et al, 2016;Beck, 2017a;Abello and Candela, 2019;Zimicz and Goin, 2020), and isolated tarsals tentatively referred to this taxon suggest australidelphian affinities (Beck et al, 2014). Thus, the pupose of these accounts is to summarize what appear to be plausibly supported clades on the basis of all available evidence, and to summarize available craniodental character support (or the lack thereof) as documented in this monograph.…”

“…Some of these studies found only relatively weak support for monophyly of Eomarsupialia over alternative topologies, but the phylogenomic study of Duchêne et al (2018) strongly supported this clade, and four uncontradicted retrotransposon insertions also provide statistically significant support (p = 0.0123) for Eomarsupialia (Nilsson et al, 2010;Gallus et al, 2015). Although this collective evidence persuades us that Eomarsupialia is probably monophyletic, we did not enforce monophyly of this clade in our dated total-evidence analysis to avoid a priori constraints on taxa with uncertain relationshipsin particular †Yalkaparidon, which fell within Eomarsupialia in the total-evidence analysis of Beck et al (2016), but not in other published analyses (Beck et al, 2014;Abello and Candela, 2019;Zimicz and Goin, 2020).…”

“…However, isolated tarsals tentatively referred to †Yalkaparidon by Beck et al (2014) show greater derived similarities to australidelphians than to paucituberculatans, and Beck et al's (2014) accompanying phylogenetic analyses also supported australidelphian affinities for this taxon (see also Beck et al, 2016). Nevertheless, the subsequent phylogenetic analyses of Beck (2017a) and Zimicz and Goin (2020), which included †Yalkaparidon and used character scores from these referred tarsals also placed this taxon in a clade with paucituberculatans (including argyrolagids, a fossil group not been included in our study; but see Abello and Candela, 2019). Although worthy of further investigation, we suspect that placement of †Yalkaparidon in a clade with paucituberculatans largely reflects convergent acquisitions of a gliriform lower incisor.…”

“…Instead we included three well-preserved Paleocene fossil metatherians: †Pucadelphys andinus, †Mayulestes ferox and †Allqokirus australis. These three taxa consistently fall outside Marsupialia, and more distant from the crown-clade than either †Herpetotherium or †Mimoperadectes, in recent phylogenetic analyses (see Rougier et al, 1998;Luo et al, 2003;Asher et al, 2004;Rougier et al, 2004;Ladevèze and Muizon, 2007;Sánchez-Villagra et al, 2007;Beck et al, 2008a;Horovitz et al, 2008;Forasiepi, 2009;Horovitz et al, 2009;Ladevèze and Muizon, 2010;Luo et al, 2011;Beck, 2012;Williamson et al, 2012;Beck et al, 2014;Engelman and Croft, 2014;Forasiepi et al, 2014a;Williamson et al, 2014;Rougier et al, 2015;Suarez et al, 2015;Ni et al, 2016;Wilson et al, 2016;Beck, 2017a;Carneiro and Oliveira, 2017b;Carneiro and Oliveira, 2017a;Maga and Beck, 2017;Bi et al, 2018;Carneiro et al, 2018;Engelman et al, 2018;Muizon et al, 2018;Abello and Candela, 2019;Carneiro, 2019;Rangel et al, 2019;Ladevèze et al, 2020; the phylogenetic analysis of Goin et al [2006] is a notable exception). All three are represented by exceptionally complete cranial material (Muizon, 1994;Marshall and Muizon, 1995;…”