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Adaptive landscapes unveil the complex evolutionary path from sprawling to upright forelimb function and posture in mammals [1]

['Robert J. Brocklehurst', 'Museum Of Comparative Zoology', 'Department Of Organismic', 'Evolutionary Biology', 'Harvard University', 'Cambridge', 'Massachusetts', 'United States Of America', 'Magdalen Mercado', 'Committee On Evolutionary Biology']

Date: 2025-07 

The ‘sprawling-parasagittal’ postural transition is a key part of mammalian evolution, associated with sweeping reorganization of the postcranial skeleton in mammals compared to their forebears, the non-mammalian synapsids. However, disputes over forelimb function in fossil synapsids render the precise nature of the ‘sprawling-parasagittal’ transition controversial. We shed new light on the origins of mammalian posture, using evolutionary adaptive landscapes to integrate 3D humerus shape and functional performance data across a taxonomically comprehensive sample of fossil synapsids and extant comparators. We find that the earliest pelycosaur-grade synapsids had a unique mode of sprawling, intermediate between extant reptiles and monotremes. Subsequent evolution of synapsid humerus form and functional traits showed little evidence of a direct progression from sprawling pelycosaurs to parasagittal mammals. Instead, posture was evolutionarily labile, and the ecological diversification of successive synapsid radiations was accompanied by variation in humerus morphofunctional traits. Further, synapsids frequently evolve toward parasagittal postures, diverging from the reconstructed optimal evolutionary path; the optimal path only aligns with becoming increasingly mammalian in derived cynodonts. We find the earliest support for habitual parasagittal postures in stem therians, implying that synapsids evolved and radiated with distinct forelimb trait combinations for most of their recorded history.

Data Availability: All data needed to replicate the analyses (landmark coordinates and functional metrics for each specimen, as well as time-dated supertrees) are available in the Supplement. All code needed to analyze the data is available in the supplemental .zip file S1 Data and is based on existing R packages. For replicating raw data collection, custom code for placing landmarks based on the existing R package Morphomap is available as part of S1 Data . 3D models of fossil humeri have been archived with the museum collections which house the original specimens and are available either from those museums (see S8 Table for contacts) or through Morphosource ( https://www.morphosource.org/projects/000609110?locale=en ).

Given the differing biomechanical requirements of sprawling versus parasagittal locomotion [ 15 , 26 , 27 ] and the historical perception of a progression toward therian parasagittal posture [ 5 , 12 , 13 ], we tested the following hypotheses: (1) Humeri from sprawling and parasagittal extant taxa occupy different adaptive optima, each maximizing traits most relevant to their specific limb posture and gait; (2) “Pelycosaurs”, the earliest-diverging NMS, share an adaptive optimum with extant sprawling taxa; (3) Increasingly derived grades of NMS shift their adaptive landscapes toward extant therians as they achieve more parasagittal postures; and (4) Evolutionary changes in NMS morphology, functional traits, and posture follow an optimal pathway from sprawling to parasagittal. Our data reveal morphological and functional trait similarities between NMS and extant comparative taxa, but also some key differences. We find that certain performance traits strongly correlate with posture, whereas others relate to different aspects of forelimb function. Recovered patterns show that postural evolution within Synapsida was complex, and the ‘sprawling-parasagittal’ transition was characterized by homoplasy and functional variation within individual synapsid clades, indicative of multiple adaptive radiations of NMS. Morphofunctional traits consistent with fully parasagittal posture evolved late in the evolutionary lineage of mammals, and so for the majority of synapsid history, the forelimbs were characterized by patterns of variation in form, function, and posture that are distinct from what we see in therians today.

Here, we use the forelimb, particularly the humerus, as a lens to study postural evolution in synapsids. Forelimb modifications were key to the evolutionary success of synapsids, including mammals [ 7 , 8 , 14 – 16 ], and the humerus provides an important window into forelimb function and posture: it is the primary articulation point between the forelimb and body, anchors the major muscle groups that drive locomotion, and its arc of motion directly impacts limb movements [ 10 , 19 – 21 ]. Further, isolated humeri preserve well in the fossil record and so allow for more extensive taxonomic sampling to produce a comprehensive evolutionary viewpoint on the ‘sprawling-parasagittal’ transition. We analyze humerus shape and functional traits across >200 extant and extinct taxa using the integrative analytical framework of evolutionary adaptive landscapes [ 18 , 19 , 22 ]. This framework links form to functional performance across multiple traits, permitting inference between morphology and higher-level functions such as limb posture or locomotion [ 19 , 23 ], and accurately captures the evolution of functional tradeoffs [ 24 ]. We extend this synthesis with Pareto optimality analyses [ 25 ] to examine how synapsids transitioned between performance peaks and adaptive optima throughout their evolution and across the ‘sprawling-parasagittal’ postural shift.

Although the synapsid ‘sprawling-parasagittal’ transition was a key event in mammalian evolution, its precise nature remains controversial [ 5 , 12 – 15 ]. Historical studies portrayed synapsid evolution as a stepwise, linear progression toward the therian condition, but often disagreed over when and how major anatomical changes translated into functional or postural change [ 5 , 12 , 13 ]. These issues primarily arose because previous authors focused on “exemplar” fossil taxa at different key nodes in the synapsid phylogeny and were restricted to qualitative functional interpretations of bony morphology. Recently, more taxonomically comprehensive morphometric work on the synapsid forelimb suggests a pattern of successive evolutionary radiations, with major synapsid groups exploring distinct morphologies and presumed functions [ 14 , 16 ]. However, to date, few studies on synapsid postcrania have incorporated explicit links between form and function into an analytical framework [ 17 , 18 ], a crucial step in characterizing the origins of therian-like limb posture and parasagittal locomotion.

The evolution of mammals is an iconic transition in the history of life that involved the profound modification of key body systems—feeding [ 1 ], hearing [ 2 ], integument [ 3 ], and metabolic physiology [ 4 ]. The exceptionally rich fossil record of mammals and their stem lineage, the non-mammalian synapsids (NMS), documents the assembly of these traits in great detail over some 300 million years [ 5 , 6 ]. Of particular interest is the dramatic reorganization of the ancestral synapsid postcranial musculoskeletal system, including regionalization of the backbone; simplification of the shoulder girdle; evolution of novel joint types (e.g., ball-and-socket shoulder, trochlear elbow); major restructuring of the limb musculature; and reorientation of the limbs from a horizontal to vertical plane [ 7 – 11 ]. These broad-scale anatomical transformations are intimately associated with a functional shift in limb posture and locomotion, from sprawling pelycosaur-grade synapsids to parasagittal therian mammals.

Contrary to expectations that synapsids would follow a consistently optimal path toward a more therian morphology, our results based on reconstructed landscapes for major nodes show statistically significant fluctuations in optimality across the major synapsid groups (with marginally non-significant effects of centroid size; RPPP ANOVA, p < 0.05, see S7 Table ). This pattern is driven by individual subclades branching off to explore both more and less optimal regions of morphospace ( Figs 6 and S10 ). Pelycosaurs undergo a small radiation but are mostly restricted to regions of high optimality that connect their adaptive peak with that for the reconstructed therapsid ancestor ( Fig 6 ). Therapsids have lower optimality than pelycosaurs, as several clades—biarmosuchians, gorgonopsians, and therocephalians—explore parts of morphospace with lower optimality on the landscape connecting Therapsida with Cynodontia ( Figs 6 and S10 ). Dinocephalians and anomodonts both exhibit greater Pareto optimality on this landscape, clustering around the inferred Therapsida optimum ( Figs 6 and S10 ). Basal cynodonts and eucynodonts generally occupy regions of lower Pareto optimality, but certain taxa evolve toward distinct peaks on the cynodont-prozostrodont landscape, with some species evolving toward the reconstructed ancestral cynodont optimum, associated with more robust humeri, and others evolving toward the prozostrodont optimum, associated with more gracile humeri ( Fig 6 ). Finally, prozostrodont cynodonts and mammaliaforms also occupy sub-optimal regions, although there does seem to be a shift in morphospace occupation toward the optimum reconstructed for ancestral therians ( Figs 6 and S10 ).

To determine whether synapsids followed “optimal” paths through morphospace over the course of their evolution as they transitioned from one adaptive optimum to another, we calculated Pareto optimality landscapes [ 25 , 46 ]. Trade-offs necessarily occur between high fitness on different landscapes due to differences in the underlying functional traits being optimized. Pareto optimality finds points in morphospace whose height on one landscape is maximized, given their height on another landscape [ 25 , 47 ]. By combining adaptive landscapes reconstructed for major nodes in the synapsid phylogeny, we determined if taxa evolve optimally through morphospace from an ancestral peak to that of the next more derived taxonomic group (see Methods ). Deviation from high Pareto optimality implies exploration of novel morphologies and functions, and either the presence of new functional drivers distinct from those along the synapsid backbone or the weakening of functional constraints and lowering of restrictions on limb evolution over time [ 25 ].

In line with the complex series of shifts recovered by SURFACE ( Figs 5 and S9 ), we found the best fitting a priori models were those with additional subgroup optima within the major synapsid grades. By contrast, models with only three regimes—here corresponding to proposed sprawling, intermediate and parasagittal postural groups [ 5 , 12 , 13 ]—are poor fits to the data (see S6 Table for detailed model comparisons). Once again, we interpret these results as evidence for synapsid evolution as a sequence of radiations, with both functional and postural variation within and between groups.

Our analyses reconstruct ancestral humeri at the base of Synapsida with traits consistent with sprawling postures, which persist throughout the pelycosaur and early therapsid parts of the tree ( Figs 4D and 5 ). Pelycosaurs, dinocephalians, and most anomodonts have humeri with very negative scores on the transitional landscape, providing strong evidence for sprawled postures ( Figs 5 and S8 ). Although our analysis indicates a sprawled ancestor for Therapsida with monotreme-like traits, several early therapsids show less negative scores (e.g., Hipposaurus, Tiarajudens), more in-line with modern reptile values, possibly indicative of differences in locomotion (e.g., faster limb movements and different kinematics) ( Figs 4D , 5 , and S8 ). We also recovered a shift toward intermediate postural scores in theriodont therapsids: the gorgonopsians and therocephalians ( Figs 5 and S9 ). Although these groups have humeri with distinctly higher transitional landscape scores than earlier synapsids, their scores are generally still negative, like modern reptiles. Another shift on the transitional landscape occurs at the origin of Cynodontia, with most taxa possessing intermediate postural scores ( Figs 4D , 5 , S8 , and S9 ). However, there is considerable heterogeneity within cynodonts and later mammaliaforms, with taxa evolving humeri with both more negative (e.g., Chiniquodon, Exaeretodon) and more positive scores (e.g., Massetognathus, Probainognathus) ( Figs 5 and S8 ). By contrast, within crown mammals, the two stem therians (Adalatherium and Gobiconodon) both scored positively on the transitional landscape ( Fig 5 ).

We find statistically significant differences in postural scores between taxonomic groups with no statistical effect of centroid size (RRPP ANOVA, p < 0.05, see S5 Table ). As expected, therians had the highest scores, and monotremes had the lowest, indicating trait combinations most and least associated with parasagittal postures respectively ( Fig 4C and 4D ). Herptiles were intermediate between monotremes and therians, due to sharing morphofunctional traits with both groups (humeral torsion with monotremes, and long humeri with therians), but still had negative scores indicating greater association with sprawling locomotion ( Fig 4D ). These results are consistent with hypothesis 1. Thus, the transitional landscape helps to conceptualize posture as a continuous variable; sprawling and parasagittal represent extremes, but we also show the great variation present within sprawlers and multiple paths between different postural groups [ 20 , 44 , 45 ]. Ancestral state reconstruction recovers the ancestor of crown-mammals as closer to therians than monotremes ( Fig 5 ). Consequently, extant sprawling monotremes do not retain a plesiomorphic state for Synapsida but have rather converged on a suite of morphofunctional characters that resemble ancestral, sprawling synapsids. This convergence may have been facilitated by the incomplete acquisition of therian characters in early mammals and their close relatives (e.g., retention of humeral torsion in taxa such as Brasilodon, Morganucodon, and Gobiconodon).

To further investigate patterns of humeral transformation toward (or away from) the therian condition during the evolution of Synapsida, we created a transitional ‘sprawling-parasagittal’ landscape. We first created a composite “sprawling” landscape by combining the independently calculated landscapes for different sprawling groups ( Fig 4A and see Methods ). Then, for each point in morphospace, we subtracted the height on the “sprawling” landscape from the height on the therian (i.e., “parasagittal”) landscape ( Fig 4B ) to create the transitional landscape ( Fig 4C ). Transitional landscape scores indicate the relative performance of different humerus morphotypes for sprawling versus parasagittal limb functions, given the many-to-one mapping that exists between humeral traits and posture [ 20 , 36 , 44 ]. We plotted our taxa on this new ‘sprawling-parasagittal’ landscape ( Fig 4C and 4D ), determined their adaptive score (height), mapped these scores onto a phylogeny and reconstructed ancestral states using maximum likelihood ( Fig 5 ). As with our functional traits, we used SURFACE and mvMORPH to test for evolutionary shifts both a posteriori and a priori in transitional landscape score within Synapsida and compared models of postural evolution in this group (see Methods ).

Searching for shifts in how functional trait weightings may have evolved using SURFACE matched those from the ancestral state reconstruction for the backbone of the synapsid phylogeny ( Figs 2 and S6 ). This analysis also recovered additional shifts within synapsid sub-groups, or along individual branches ( S6 Fig ). Fitting of different evolutionary regimes to the data using mvMORPH found historical hypotheses of morphofunctional shifts within synapsids [ 5 , 12 , 13 ] are significantly outperformed by more complex models featuring additional optima for subgroups within the major synapsid grades (see S4 Table for detailed model comparisons). These results are more consistent with the view of synapsid evolution as a sequence of radiations, with functional differentiation within and between each major grade.

Individual NMS vary substantially in how different functional traits are optimized on their landscapes ( Figs 2B , 3 , S6 , and S7 ). Pelycosaurs primarily emphasize humeral torsion, consistent with their reconstructed sprawling posture [ 42 , 43 ]. Other traits—‘spin’ leverage, ‘swing’ force, and humeral strength—also contribute to the pelycosaur landscape with varying importance across taxa ( Figs 3 and S7 ). Pelycosaurs differ significantly in terms of trait weighting from herptiles, contra hypothesis 2, but not from monotremes (see S3 Table ). Therapsids differ in functional trait optimization across subclades ( Figs 2B , 3 , S6 , and S7 ). The biarmosuchian Hipposaurus emphasizes torsion and humeral length, similar to herptiles. Dinocephalians and anomodonts predominantly optimize strength and muscle force leverages. Gorgonopsians and therocephalians optimize humeral length, but whereas gorgonopsians emphasize ‘swing’ torque and strength, therocephalians put more importance on humeral torsion ( Figs 3 and S7 ). Cynodonts show substantial variability in trait optimization, but generally emphasize either humerus length, or a combination of strength and muscle force leverages ( Figs 2B , 3 , S6 , and S7 ). Most cynodonts do not optimize humeral torsion, but there are some exceptions including among derived prozostrodonts and mammaliaforms ( S6 and S7 Figs ). This contrasts with therian trait optimization, as well as that reconstructed along the synapsid backbone—the importance of torsion in these taxa may represent independent instances of trait diversification. As with humerus shape, the mean trait weightings of each successively derived NMS grade become more similar to the therian condition, in support of hypothesis 3. However, within each grade, there is substantial variation in trait optimization, which does not support the idea of a series of stepwise shifts toward therians.

In addition to individual adaptive landscapes for each specimen, we calculated adaptive landscapes for major taxonomic groups within our dataset; here, the group mean is maximized on the resulting landscape. Extant species optimize different combinations of functional traits ( Figs 2 , 3 , and S6 ), in support of hypothesis 1. Herptiles strongly emphasize humerus length and humeral torsion ( Fig 3 ), traits associated with increasing stride length in sprawling tetrapods [ 34 , 35 ], as well as high-velocity advantage for humeral ‘swing’ ( Fig 3 ), resulting in relatively fast limb movements and greater muscle working range [ 15 ]. Monotremes show high weighting for humeral torsion, ‘spin’ muscle leverage, and bending strength ( Fig 3 ), reflective of both their sprawling posture and semi-fossorial lifestyle [ 15 , 36 – 38 ]. Therians optimize humerus length, radius of gyration, and ‘swing’ muscle force leverage for rotating the limb through an arc ( Fig 3 ). Longer length and a shorter radius of gyration are associated with more efficient locomotion [ 39 , 40 ], whereas increasing muscle leverage for planar rotation would result in more powerful movements of the limb in the parasagittal plane [ 15 , 41 ].

Species-level analysis of trait weights shows considerable variation across groups (RRPP MANOVA, p < 0.05, r 2 = 0.39, see S3 Table ), but also within major groups, especially within NMS ( Figs 2B and S6 ). Centroid size also showed a statistically significant, but smaller, effect on trait weightings (RRPP MANOVA, p < 0.05, r 2 = 0.11, see S3 Table ), and is likely important in structuring within-group variation. Examining adaptive landscapes based on ancestral-state reconstructions of humerus shape along the backbone of the synapsid phylogeny ( Fig 2C ) reveals the relative importance of individual traits through synapsid evolution, semi-independent of clade- or taxon-specific patterns. The reconstructed ancestral landscape for the Synapsida node heavily optimizes humeral torsion, as well as ‘spin’ muscle leverage, and this combination remains stable throughout early synapsid evolution. The landscape changes at the base of Theriodontia (gorgonopsians, therocephalians, and cynodonts), and throughout Cynodontia, with an increase in optimization for humeral length, ‘swing’ force leverage and a decrease in weighting for torsion ( Fig 2C ). Notable changes to the reconstructed landscapes occur prior to the origins of prozostrodontian cynodonts and Mammaliaformes: increased optimization for humeral length, radius of gyration, and ‘swing’ force leverage, with less of an emphasis on humeral torsion and ‘spin’ leverage ( Fig 2C ).

Function was inferred by measuring seven osteological proxies—bone length, radius of gyration (an important inertial property), torsion, bending strength, and muscle force and speed leverage—for each humerus in our sample (see Methods and S4 Fig ). Muscle leverage was separated into two components; ‘swing’ refers to motion of the limb through a horizontal or vertical arc during locomotion, and ‘spin’ refers to long-axis rotation of the limb [ 15 ]. We interpolated the measured functional traits across the morphospace [ 31 ], to produce seven distinct performance surfaces that illustrate the co-variation of humerus shape with each functional trait ( Fig 2A ). Performance surfaces were combined to produce adaptive landscapes for each species in the dataset using combinatorial optimization, weighting functional traits to maximize each species’ height on their resulting landscape [ 18 , 19 , 22 ]. Combinations of trait weights that produced optimal landscapes were then compared across taxa and along the synapsid phylogeny using ancestral state reconstructions ( Fig 2B and 2C ). Evolutionary shifts in functional trait weighting were identified using the SURFACE algorithm [ 32 ], and specific a priori hypotheses based on previous studies of synapsid locomotor evolution [ 5 , 12 , 13 ] (see S5 Fig ) were tested against each other using mvMORPH [ 33 ] (see Methods ).

In therapsids, this variation is partitioned across different subclades. Anomodonts and dinocephalians generally plot with pelycosaurs or closer to monotremes. The biarmosuchian Hipposaurus, our earliest-branching therapsid, plots within herptiles, gorgonopsians plot on the outer edges of the therian and herptile spaces, and therocephalians plot close-to or within the therian cluster ( Fig 1C ). Basal cynodonts generally occupy the central region of morphospace, as do the two more derived eucynodont subclades, cynognathians and probainognathians, but in both subclades some species independently move into the therian region of morphospace (see S3 Fig ). Some mammaliaforms—Eozostrodon and Megazostrodon [ 29 ]—fall within therian morphospace, but others—Borealestes [ 30 ]—do not ( Figs 1C and S3 ). The two stem therians included here fall well within the range of extant, crown-therian morphologies ( Figs 1A and S3 ). While the overall mean humerus shape of each successive NMS radiation—pelycosaurs, therapsids, and cynodonts—gets closer to the mean therian shape (see pairwise distances in S2 Table ), as outlined by hypothesis 3, there is considerable variation around these mean shape values.

Pelycosaurs, the earliest grade of NMS, occupy the region of morphospace between herptiles and monotremes—contra hypothesis 2—while overlapping neither, consistent with their “basal” phylogenetic position, and a unique sprawling posture [ 13 , 28 ] (significant pairwise differences between means, pelycosaurs versus herptile p < 0.05, pelycosaurs versus monotremes p < 0.05, see S2 Table ). Other non-synapsid fossil taxa also plot in this part of morphospace (e.g., Eryops, Orobates, Seymouria [ 20 , 22 ]), indicating pelycosaur humeri do not deviate strongly from a general early crown-tetrapod condition. However, more derived grades of NMS—therapsids and cynodonts—diversify into much larger regions of morphospace and exhibit greater variation in humerus shape ( Figs 1A , 1C , and S3 ).

To capture morphological evolution of the humerus throughout synapsid evolution, we measured humeri from 70 fossil taxa and compared them to 141 extant quadrupedal tetrapods including amphibians, reptiles, and mammals (see S1 Table and S1 Fig ). Shape variation was quantified using a novel, homology-free pseudo-landmarking approach to generate 3D coordinates along the surface of each bone (see Methods and S2 Fig ). Procrustes aligned landmarks were ordinated using between-groups principal components analysis (bgPCA) to differentiate postural groups (sprawling versus parasagittal versus unknown for fossils) and produce a morphospace ( Fig 1 ). Regarding our first hypothesis, humeri of major extant groups fall in distinct regions of morphospace (Procrustes ANOVA and pairwise comparisons, p < 0.05, see S2 Table ), but the main axis of shape variation (bgPC1) does not separate them based on posture. Instead, bgPC1 differentiates the relatively gracile humeri of parasagittal therian mammals and sprawling “herptiles” (non-avian reptiles plus amphibians), from the robust humeri of sprawling monotremes and moles ( Fig 1A and 1B ). Therians separate from herptiles along the second axis of variation (bgPC2), which reflects differences in the offset between the proximal and distal ends of the humerus, curvature of the humeral shaft and relative width of the proximal versus distal ends of the humeral epiphyses ( Fig 1A and 1B ).

Discussion

The evolution of parasagittal posture in mammals and their ancestors has been studied for over a century, but previous efforts to understand changes to the limbs and locomotion have historically lacked taxonomic scope and an appropriate analytical framework [5,12,13]. Here, we used evolutionary adaptive landscapes [18,22] to predict relationships between humerus morphology, functional traits, and posture to develop a predictive framework to illuminate the ‘sprawling-parasagittal’ transition in synapsids. Based on differences in locomotor biomechanics, we expected the humeri of extant taxa to group together in morphospace based on posture (Hypothesis 1). Although parasagittal therians group separately from other taxa, sprawling reptiles and amphibians (“herptiles”) do not group with sprawling monotremes. Together with therians, herptiles share relatively long, gracile humeri (Figs 1, 3, and S6), features that arose convergently in these groups despite their contrasting habitual postures. Longer humeri are likely advantageous for general terrestrial locomotion regardless of posture, although the precise selective advantages may differ (e.g., speed versus efficiency) [34,39,40]. In contrast to therians, herptiles and monotremes both emphasize humeral torsion, supporting torsion as a strong indicator of sprawling forelimb posture [35,48] (Figs 2–4). However, monotremes and herptiles optimize torsion to differing degrees and in distinct combinations with other functional traits, reflecting wide variation in sprawling locomotor kinematics (e.g., powerful long-axis rotation versus faster limb retraction) [20,36,37]. Therians are unique in emphasizing radius of gyration (Figs 2 and 3)—due to a combination of a more proximally located center of mass and reorganization of the humeral head moving the center of rotation distally—potentially indicating this trait as a signal of more parasagittal postures. These similarities and differences across diverse extant animals provide interpretive power when reconstructing forelimb function and postural evolution in synapsids.

The earliest-diverging NMS, the pelycosaurs, are traditionally reconstructed with a sprawling posture [42], and thus we hypothesized morphological and functional similarities with extant sprawlers (Hypothesis 2). Yet, our analysis shows pelycosaurs are morphologically distinct from all extant sprawling groups, and instead overlap with extinct non-synapsid tetrapods, indicating that pelycosaur humeri had not diverged from the plesiomorphic crown tetrapod condition (Fig 1). Functionally, pelycosaurs show high optimization for torsion, indicative of sprawling posture, but they optimize this trait to a more extreme degree than either reptiles or monotremes (Figs 3 and S6). Pelycosaurs also emphasize both ‘swing’ force and ‘spin’ muscle leverage, which aligns with previous work demonstrating coupled rotations at the screw-shaped glenoid joint during a stride [13,28], as well as humeral strength. Taken together, the emphasis on torsion, strength, and muscle leverage shows pelycosaurs used slow, forceful limb movements, combining humerus long-axis rotation and retraction. This combination contrasts with reptiles, which are adapted for (relative) speed [15], and monotremes, which use almost exclusively long-axis rotation [36,37]. Our analyses thus indicate pelycosaurs possessed distinct humerus morphologies and combinations of functional traits not represented by modern taxa [18], and it was from this unique starting point that mammalian posture ultimately evolved.

Based on historical interpretations of the synapsid fossil record [5,12,13], we expected a trend toward more therian-like morphologies and functional traits in more derived NMS, reflecting more parasagittal postures (Hypothesis 3). Although this general pattern was broadly supported, we also found significant variations on this theme (Figs 1–3). Our transitional ‘sprawling-parasagittal’ landscape strongly supports monotreme-like sprawling postures in dinocephalian and anomodont therapsids (Figs 4 and 5), with these clades showing increased optimization for strength and muscle force leverages at the expense of humerus length (Figs 2, 3, S6, and S7). This combination of functional traits is potentially related to the acquisition of larger body sizes in both groups [49,50], and fossorial behaviors in smaller dicynodonts [51–53], as seen in modern monotremes and talpid moles [36,37,54]. Similar ecomorphological convergence in the forelimb has been previously noted between fossorial and large-bodied mammals [14]. We argue that the co-occurrence of large body sizes and strong humeri in dinocephalians and anomodonts is indicative of non-parasagittal postures in these groups. Modern large-bodied therians can compensate for size-related bending stresses by changing limb posture, from more crouched to more erect [26]. Sprawling taxa, on the other hand, must accommodate size-related stresses by increasing limb bone robusticity, resulting in “overbuilt” limb bones [27,55].

Other therapsid groups had diverging scores on the ‘sprawling-parasagittal’ transitional landscape. Biarmosuchians, the earliest branching therapsids and represented here by Hipposaurus, experienced a shift on the transitional landscape away from monotremes and toward reptiles (Figs 4, 5, S8, and S9). Specifically, Hipposaurus overlaps with reptiles in morphospace and optimizes humeral torsion, length and ‘swing’ speed (Figs 1 and 3), indicating a reptile-like sprawling posture and kinematics [20]. Although this combination suggests adaptations for relatively fast limb movements, it may not be reflective of the ancestral therapsid condition, due to a persistent ghost-lineage following their divergence from pelycosaurs [56,57]. Later theriodont therapsids, the gorgonopsians and therocephalians, experienced similar but less extreme shifts on the transitional landscape, sitting on the outskirts of the reptile and therian regions of morphospace (Figs 4, 5, S8, and S9). Therocephalians share similar functional traits to Hipposaurus, but gorgonopsians combine humerus length with ‘swing’ force and strength. These morphofunctional traits are indicative of more active, predatory lifestyles in the three clades [58–61], but further suggest that gorgonopsians may have engaged in unique behaviors with their forelimbs (e.g., grappling large prey similar to more recent carnivores [62]). Therocephalians and gorgonopsians both have average clade-wise postural scores converging on reptiles, but several taxa (Gorgonops, Olivierosuchus) have higher scores closer to therians (S8 Fig). This convergence may reflect more parasagittal postures in these taxa, but the range of forelimb poses would have been constrained by the therapsid shoulder girdle, with its caudolaterally facing glenoid [5].

Following theriodonts, further morphofunctional transformations to the forelimb associated with increasingly parasagittal postures have been proposed for cynodonts [5,13]. Cynodonts do shift closer to therians on the transitional landscape, but this movement is accompanied by considerable variation (Figs 1, 4 and S8) and evolutionary heterogeneity (Figs 5 and S9). Whereas postural trait variation in therapsids is phylogenetically structured by clade, in cynodonts it is more widespread across the phylogeny, implying enhanced evolutionary lability in posture and forelimb use. For functional traits, cynodonts generally optimize either humerus length, or a combination of strength and muscle force leverages (Figs 2, 3, S6, and S7), possibly reflecting adaptations to distinct, specialized ecologies (e.g., digging [63]). Most cynodonts are not optimized for humeral torsion, but those that are (e.g., Lumkuiia, Riograndia, Brasilodon) have been previously reconstructed with sprawling postures [64–66]. Likewise, lower torsion might indicate less sprawled postures in other taxa [67]. Postural scores in cynodonts are mainly in-line with modern reptiles, but some taxa achieve higher, more therian postural scores (Massetognathus, Probainognathus) (Figs 5 and S8). Given the disparity in cynodont forelimb functional and postural traits, it is likely that different species employed different postures, but were still constrained by the shoulder girdle to non-parasagittal (i.e., sprawling to semi-sprawling) limb poses [13,67–69]. Cynodont forelimb disparity is further explored by mammaliaforms, which possess disparate postural scores and functional traits: humerus length in Megazostrodon; length and torsion in Morganucodon; and length, ‘spin’ leverage and strength in Borealestes (Figs 2 and S7). The functional, and likely postural, diversity of mammaliaform humeri reflects the great ecomorphological disparity present in this group [70].

Our comprehensive survey of NMS found evidence of therian traits evolving multiple times, but limited support for fully parasagittal postures. Previous hypotheses place the origin of parasagittal posture in crown Mammalia [12] or even Theria [13]. Our two stem therians (Adalatherium and Gobiconodon) both plot with crown therians in morphospace (Figs 1 and S3) and on the transitional landscape (Figs 4 and 5). However, when we examine humerus traits, we find Gobiconodon strongly optimizes humeral torsion, which would preclude it from adopting a habitually parasagittal posture [71] (Figs 2 and S7). Adalatherium, on the other hand, possesses a functionally therian humerus, optimizing length, ‘swing’ force leverage and, to a lesser extent, inertial properties. Further support for therian parasagittal posture in Adalatherium comes from other aspects of the forelimb skeleton: the scapula has a ventrally facing glenoid facet, the coracoid portion of the glenoid fossa faces caudo-ventrally not laterally, and the ulna has a well-developed trochlear notch which likely restricted elbow motion to a single plane [72]. A similar condition in multituberculates, in combination with low humeral torsion, has been interpreted as evidence these taxa were also parasagittal [73,74]. Therefore, our results support the origins of fully parasagittal posture within stem therians [13], making it a late innovation in the grand scheme of synapsid evolution. Additionally, due to uncertainty in the phylogenetic arrangement of gondwanatherians (e.g., Adalatherium), eutriconodonts (e.g., Gobiconodon) and multituberculates [75,76], it is possible that adaptations for more parasagittal postures arose multiple times independently along the therian stem.

From evolutionary theory, we predicted that throughout their complex evolutionary journey, NMS were following an optimal pathway through morphospace (Hypothesis 4). Following prior work on synapsid evolution [5,12,13], we assumed that this optimal pathway would correspond to the acquisition of increasingly therian traits and postures. Instead, our Pareto optimality analyses clearly illustrate synapsid evolution as a series of successive adaptive radiations (Figs 6 and S10), with taxa repeatedly evolving away from the reconstructed optimal pathway. Pelycosaurs represent the first radiation of synapsids, but they do not diversify the forelimbs to the same extent as later synapsid grades [16]. The second radiation at the origin of Therapsida corresponds to a proposed morphofunctional shift in synapsid evolution based on important morphological transformations like the change in the scapular glenoid from a screw-shape to a more mobile hemi-sellar shape [5,12]. The removal of morphofunctional constraints on the forelimb potentially facilitated therapsid diversification, as they explored novel regions of morphospace [16] and experimented with novel forelimb functions [52,61,77] (Figs 1–3 and S7). Some clades diversified in areas of high Pareto optimality (e.g., anomodonts), but biarmosuchians and theriodont therapsids explored Pareto suboptimal regions of morphospace and combinations of functional traits closer to those seen in therians and reptiles. This variability gives Therapsids a lower average Pareto optimality than pelycosaurs, providing strong supporting evidence for reduced evolutionary constraints [25]. Recovering theriodont therapsids as Pareto suboptimal also demonstrates that becoming increasingly therian was not the ‘optimal’ evolutionary pathway for synapsids until much later in their history.

Contrary to therapsids, cynodonts and mammaliaforms evolve on a multi-peak Pareto landscape, with optima corresponding to more robust and gracile humeri associated with the ancestral Cynodontia and derived Prozostrodontia landscapes, respectively (Figs 6 and S10). However, only a few taxa occupy either of these optimal regions, with most cynodonts and mammaliaforms occupying Pareto suboptimal regions between the peaks. We propose that the two peaks, representing distinct humerus morphologies and functional traits, constitute two ends of an ecological spectrum (e.g., fossorial to scansorial [64,65]), with more generalist taxa falling in the center due to conflicting selective pressures [24]. The gracile peak on the prozostrodont Pareto landscape is closer to the therian optimum and forms a Pareto optimal evolutionary pathway toward Theria. However, this is not the only optimal path on this landscape, as moving back toward the ancestral cynodont peak is also Pareto optimal. These multiple optima may have facilitated the disparate evolution of mammaliaforms [70], and the opposing evolutionary trajectories of monotremes and therians. Monotremes convergently re-evolve toward the robust, ancestral cynodont optimum, and therians realize a new set of humerus morphologies and functions. Accompanied by modifications to other aspects of the therian forelimb skeleton along the therian stem [72]—a mobile scapula, ventrally facing glenoid, and hinge-like elbow joint—this new morphology presumably removed the final barriers to achieving a habitually parasagittal forelimb posture [15].

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