Phylogeny, function and ecology in the deep evolutionary history of the mammalian forelimb

Abstract

Mammals are the only living members of the larger clade Synapsida, which has a fossil record spanning 320 Ma. Despite the fact that much of the ecological diversity of mammals has been considered in the light of limb morphology, the ecological comparability of mammals to their fossil forerunners has not been critically assessed. Because of the wide use of limb morphology in testing ecomorphological hypothesis about extinct tetrapods, we sought: (i) to estimate when in synapsid history, modern mammals become analogues for predicting fossil ecologies; (ii) to document examples of ecomorphological convergence; and (iii) to compare the functional solutions of distinct synapsid radiations. We quantitatively compared the forelimb shapes of the multiple fossil synapsid radiations to a broad sample of extant Mammalia representing a variety of divergent locomotor ecologies. Our results indicate that each synapsid radiation explored different areas of morphospace and arrived at functional solutions that reflected their distinctive ancestral morphologies. This work counters the narrative of non-mammalian synapsid forelimb evolution as a linear progression towards more mammalian morphologies. Instead, a disparate array of early-evolving shapes subsequently contracted towards more mammal-like forms.

Musculoskeletal modelling of sprawling and parasagittal forelimbs provides insight into synapsid postural transition

“…With the origin of therapsids, the glenoid joint lost its craniocaudal screw-shape, instead becoming a dorsoventrally-oriented notch [5]. However, most early-branching and large bodied therapsids, including dinocephalians and anomodonts, retained laterally expanded humeral epiphyses [9,35] (figure 5). While ROM is predicted to be higher than in 'pelycosaurs' because of changes to the glenoid joint, the expanded humeral epiphyses would still restrict ROM to some extent, as demonstrated in the echidna (figure 2).…”

“…Although glenoid morphology remains notch-like in mammaliaforms [7], there is some diversity in the 'openness' of the facet [37], and considerable variation in humeral shape [35]. Indeed Mesozoic mammaliaforms explored several new niches not seen in non-mammalian cynodonts [37,38], additional evidence that forelimb-use and ROM is not necessarily inhibited by the possession of hemi-sellar joints.…”

“…Although historically compared to lepidosaurs [8,34], 'pelycosaurs' share aspects of their forelimb functional morphology with the echidna; restricted glenohumeral ROM, emphasis on humeral long-axis rotation movements, and expanded epiphyses [16,34,35]. Therefore, we might expect 'pelycosaurs' to exhibit large MMAs, particularly for pronation, but not as extreme as those of the echidna which possess additional derived features, e.g., distal insertion of the m. latissimus (figures 3, 4).…”

Choice of 3D morphometric method leads to diverging interpretations of form–function relationships in the carnivoran calcaneus

“…Functional demands on the skeleton related to behaviors such as feeding and locomotion frequently lead to predictable relationships between an organism’s morphology and its ecology (Wainwright, 1991; Bock, 1994; Barr, 2018). In turn, these form–function relationships allow for the inference of behavior in species for which we have only morphological data, such as fossils (Chen and Wilson, 2015; Nations et al, 2019; Grossnickle et al, 2020; Lungmus and Angielczyk, 2021), quantification of macroevolutionary rates and modes (Kilbourne and Hutchinson, 2019; Law et al, 2019; Law, 2021; Prang et al, 2021; Slater, 2022), and the testing of hypotheses about ecological responses to competition and environmental change (Feder et al, 2010; Polly, 2010; Polly et al, 2017; Short and Lawing, 2021). A number of approaches have been used to quantify patterns of ecomorphological variation in the post-cranial skeleton, ranging from functional indices derived from linear measurements (Van Valkenburgh, 1987; Losos, 1990; Garland and Janis, 1993; Collar et al, 2013; Barr, 2014) to the description of complex patterns of 3D shape variation using the tools of geometric morphometrics (Curran, 2012; Fabre et al, 2013; Martín-Serra et al, 2014; Wang et al, 2020; Dunn and Avery, 2021).…”

Trait-based paleontological niche prediction demonstrates deep time parallel ecological occupation in specialized ant predators

“…Across vertebrate species, limb anatomy is a predictor of locomotion, prey items, and substrate behaviour. In particular, the forelimb anatomy of carnivores has been used to predict the likely predatory habits and prey size of extinct carnivorous mammals and mammaliaforms (Dunn et al 2019; Ercoli et al 2012; Figueirido et al 2016; Jenkins et al 2020; Lungmus and Angielczyk 2021; Meloro and Louys 2014). Other examples of extant morphology used in the prediction of extinct ecology include estimating prey type in extinct raptor species from present-day birds of prey (Hertel 1995); predicting prey items and modes of scavenging in extinct crocodyliforms from extant crocodyliform snout morphology (Drumheller and Wilberg 2019); approximating arboreal behaviour in extinct primates (Rector and Vergamini 2018); and predicting habitat preferences in fossil Anolis lizards using ear canal shape (Dickson et al 2017).…”