Niche partitioning shaped herbivore macroevolution through the early Mesozoic
Triassic herbivore ecomorphological feeding guildsWe use herbivorous tetrapod jaws as an ecomorphological proxy and consider variation in both shape and function. Archosauromorphs and therapsids occupy different areas of shape morphospace with almost no overlap (Fig. 1a). The main discrimination between these two clades is along the major axis of variation, principal component (PC) 1, while PC2 discriminates therapsid subgroups, but not the sauropsids, which remain clustered on PC2. This pattern of greater sauropsid conservatism relative to synapsids appears to remain consistent in morphospaces generated from combinations of the first three PCs (Supplementary Fig. 4). Two clades crosscut this general pattern: the areas of morphospace occupied by rhynchosaurs (Archosauromorpha) and procolophonoids (Parareptilia) overlap with other sauropsids as well as with therapsids (Fig. 1a). This functional-ecological discrimination between the two major tetrapod clades, including the ancestors of modern birds and crocodilians on the one hand (archosauromorphs) and mammals on the other (therapsids) helps explain how both clades survived and neither overwhelmed the other, despite evidence for arms races between both through the Triassic14,16,21.Fig. 1: Shape and functional morphospace occupation of early Mesozoic herbivores.a Shape morphospace based on geometric morphometric data. b–i Contour plot of (interpolated) functional character data mapped onto shape morphospace. Increasing magnitude of functional character values indicated by colour gradient from dark to light (scale varies across characters). j Functional morphospace based on the above functional characters. Misc., Miscellaneous pseudosuchians. MA, Mechanical advantage. Asterisk indicates tooth row length or length of the mandibular functional surface. N = 136 taxa. All silhouettes created by S.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/) and Jeff Martz (United States National Park Service), available for academic use with attribution.Full size imageContour mapping of the functional characters (Supplementary Table 1) helps to reveal how jaw shape reflects function (Fig. 1b–i). The sauropsid-therapsid division along PC1 appears closely linked with anterior (Fig. 1b) and posterior (Fig. 1c) mechanical advantage (MA) and maximum aspect ratio (MAR) (Fig. 1e), reflecting biting efficiency and speed, and jaw robusticity. PC2 reflects a more complex pattern and appears to document the opening MA (Fig. 1d), relative symphyseal length (RSL) (Fig. 1g), and articulation offset (AO) (Fig. 1i), reflecting the speed of jaw opening, anterior robusticity, and efficiency of jaw lever mechanics, respectively. These functional characters were used to generate a separate jaw ‘functional’ morphospace (Fig. 1j) in which PC contribution scores indicate that functional PC1 (fPC1) is equally dependent on posterior MA, anterior MA, and MAR, while fPC2 is dominated by the opening MA and AO (Supplementary Table 2). Taxon distribution is more extended along fPC2, but the functional morphospace shows largely the same patterns as seen in the shape morphospace (Fig. 1j and Supplementary Fig. 5). In the functional morphospace, only the rhynchosaurs overlap with therapsids, and they occupy a space between cynognathian cynodonts and dicynodonts, rather than being associated more closely with dicynodonts as in the shape morphospace (Fig. 1a).Triassic therapsid jaws were highly efficient, granting them relatively high power and speed, as shown by the shape and functional morphospaces (Fig. 1a, j). Therapsids have relatively compressed mandibles (Fig. 1a) that maximise the areas of muscle attachment, increasing MA (Fig. 1b–c). Among therapsids, eutheriodonts developed this characteristic further, diverging from other taxa in terms of the greater compression of their mandibles and the reduced offset between tooth row and jaw joint. This progression continues through the successive positions in morphospace of the bauriid therocephalians, cynognathian cynodonts and tritylodont mammaliamorphs. Relative expansion of the tooth row (Fig. 1f) and development of the jaw musculature supports therapsid optimisation for powerful bites. The more anterior positioning of the adductor musculature in dicynodonts manifests as the highest anterior and posterior MA values of any group with the quadrate-articular jaw joint. Tooth row expansion and low opening MA in eutheriodonts indicates power was directed towards oral processing/mastication, while dicynodont edentulism supports optimisation for a powerful, shearing bite22.Triassic sauropsid jaws were less efficient, but follow similar trends to therapsids in developing comminution ability. Sauropodomorphs and allokotosaurs diverged from these trends, opting for fairly quick but weak bites with relatively large tooth rows to optimise ingestion of vegetation. Aetosaurs, ornithischians and some procolophonoids exhibit morphologies that mechanically improved on the basal morphology of the sauropodomorphs and allokotosaurs, with greater MA and robusticity, although jaw closure was notably slower. This may suggest greater cropping ability and further herbivorous specialisation. Rhynchosaurs show similar trends in developing their jaw musculature, exhibiting MA values (Fig. 1b–d) that converge towards those of therapsids. Leptopleuronine procolophonids are interesting in that their jaws were very stout with slower bite speed and high MA, suggesting they were feeding on very hard/ tough materials. The expansion of the tooth row in aetosaurs, ornithischians and rhynchosaurs suggests they were emulating the eutheriodonts in developing more effective mastication. Consequently, early Mesozoic herbivores can be subdivided broadly by their preference for gut or oral processing23. Different groups of therapsids and sauropsids followed common adaptive pathways as specialised herbivores: as phylogenetic contingency combined with ecology to produce convergent forms. This pattern has already been observed among dinosaurs24 and our results suggest it runs even deeper in the tetrapod tree.Regional mapping on the functional morphospace plot (Fig. 1j) shows qualitative groupings that may reflect different functional feeding groups (FFG) or guilds. To quantitatively identify these FFGs, three separate cluster analyses were run using a distance matrix of the standardised functional data. All methods gave similar results with regards to the separation and stability of the cluster groups but disagree over the precise groups (Supplementary Table 5 and Supplementary Data 5). External validation metrics were used to assess how closely the cluster groups corresponded with broad and higher resolution taxonomic groupings (Supplementary Data 14), which highlighted the relatively strong phylogenetic control on mandibular morpho-function (Supplementary Table 6 and Supplementary Data 14). By removing inconsistent taxa and looking for consensus among the three sets of cluster results, we identified five main FFGs: the ingestion generalists (relatively unspecialised), the prehension specialists (stronger, larger bites), the durophagous specialists (slow, powerful bites), the shearing pulpers (that cut and smash plant food), and the heavy oral processors (using teeth to reduce the food). Many sauropsid taxa were recovered within the ingestion generalist FFG, and so the clustering methodology was repeated with the ingestion generalists in an effort to generate higher resolution functional feeding subgroups (FFsG) for use in analysis of potential competition (Supplementary Data 5 and 6). This allowed identification of three additional FFsG within the ingestion generalist group: the basal generalists, tough generalists and light oral processors.Dissecting the functional properties within each of the FFGs enables us to determine the likely feeding specialisations (Fig. 2 and Supplementary Data 7) and track their prevalence through geological time (Fig. 3 and Supplementary Data 8 and 9). MA is the main discriminant for our FFGs. The FFGs show that therapsid herbivores fall into three FFGs, and archosauromorphs into two groups. However, the identification of the FFsG shows that archosauromorph morpho-functional differences are more subtle than those present in therapsids, illustrating the varying levels of specialisation and phylogenetic constraints within the two clades. We note that only two FFGs include both therapsids and sauropsids, the ‘shearing pulper’ group, including both hyperodapedontine rhynchosaurs and dicynodonts, and the light oral processor subgroup of the ingestion generalists, which included both archosauromorph rhynchosaurs and trilophosaurs and bauriid therocephalians. Sauropsids show much greater FFG variability within clades than therapsids, where feeding mode is largely common to the entire clade (Fig. 2 and Supplementary Data 5 and 6). This may reflect greater ecological diversification within sauropsid clades as a result of being relatively unspecialised compared to contemporaneous therapsid herbivores, which were already quite specialised at the onset of the Mesozoic. This contrast in specialisation granted sauropsids greater freedom to diversify across different guilds, despite therapsids possessing more mechanically efficient jaws (Fig. 2).Fig. 2: Functional feeding groups. Characteristics of the different functional feeding groups with silhouettes of the taxa that exhibit these feeding modes (see Fig. 1 for silhouette key).Preference of each group for gut or oral processing/comminution of food is indicated. The strength of separation between the groups is illustrated by the darkness of the band connecting each FFG description box. Violin plots show taxon density. Box plots showing median value (centre) and upper and lower quartiles representing the minimum and maximum bounds of the boxes, with whisker illustrating standard deviation. DS durophagous specialist, HOP heavy oral processor, IG ingestion generalist, PS prehension specialist, R Relative, SP shearing pulper, SA symphyseal angle. N = 136 taxa. All silhouettes created by S.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/) and Jeff Martz (United States National Park Service), available for academic use with attribution.Full size imageFig. 3: Functional feeding groups of early Mesozoic herbivores through time.a The relative species richness of different clades through time. b The relative richness of different functional feeding groups through time. c Distribution of functional feeding groups across different taxonomic groups and subgroups of herbivores is indicated. Clade and guild changes shown at the midpoints for each stage/substage in panels a and b. Temporal ranges of the groups are based on first and last fossil occurrence dates, highlighting the span of ecological prominence for each group. Environmental changes from arid to humid shown by background colour gradient. Predominant vegetation4,60,61 and characteristic vegetation (relative) height93,94 indicated by tree silhouettes. Geological Events: PTME Permian-Triassic mass extinction, CPE Carnian Pluvial Event, TJE Triassic-Jurassic mass extinction, Timebins: ANS Anisan, CH Changhsingian, H Hettangian, I Induan, L CRN Lower Carnian, L NOR Lower Norian, LAD Ladinian, Lop Lopingian, M. NOR Middle Norian, OLE Olenekian, PLB Pliensbachian, RHT Rhaetian, SIN Sinemurian, TOA Toarcian, U. NOR Upper Norian, W Wuchiapingian, Feeding Functional Groups: BG basal generalist, DS durophagous specialist, HOP heavy oral processor, IG ingestion generalist, LOP light oral processor, PS prehension specialist, SP shearing pulper, TG tough generalist, Larger Clades: Dm Dinosauromorpha, Psd Pseudosuchia, BAm Basal Archosauromorpha, Pr Parareptilia, Th Therapsida, Taxonomic Groups: Parareptilia: OWN Owenettidae, B. PRC Basal Procolophonidae, PRCn Procolophoninae, LEP Leptopleuroninae, Therapsida: DCYN Dicynodontia, BAUR Bauriidae, CYNG Cynognathia, TRTY Tritylodontia, Archosauromorpha: ALLOK Allokotosauria, B. RHYN Basal Rhynchosauria, RHYN Rhynchosauridae, RHYN HYP Hyperodapedontinae, PSD Misc Miscellaneous Pseudosuchia, AETO Aetosauria, SILE Silesauridae, B. SPm Basal Sauropodomorpha, PLT Plateosauridae, MSP (non-sauropodiform) Massopoda, SPf (non-sauropod) Sauropodiformes, SP Sauropoda, B. ORN Basal Ornithischia, B. THY Basal Thyreophora, TRL Trilophosauria, All silhouettes created by S.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/) and Jeff Martz (United States National Park Service), available for academic use with attribution.Full size imageNiche partitioning and competition avoidanceWere different clades of herbivores apparently competing for the same resources and in the same way? It seems not. We find that differences in jaw morphology are highly constrained by phylogeny and our FFGs do closely reflect phylogenetic groupings. Such phylogenetic structuring does not preclude meaningful functional interpretation of our FFGs to study divergent feeding strategies;25,26 this simply reflects that morphology and thus functionality is highly controlled by phylogeny. The distinction between the areas of morphospace occupied by therapsids and archosauromorphs (Fig. 1a) represents their fundamentally different feeding priorities, in which archosauromorphs optimised prehension and therapsids optimised comminution. Therapsids appear to have consistently enhanced biting power, possessing greater MA than most sauropsids, and this may reflect differences in the primary jaw adductor musculature of sauropsids (pterygoideus) and therapsids (adductor mandibularis)27. Sauropsid jaw mechanics are less efficient compared to therapsids, but it is clear that sauropsids, particularly the archosaurs achieved significantly larger body sizes than therapsids16. Therefore, it appears that sauropsids favoured increasing their bite forces through boosting jaw muscle mass and the absolute power involved, rather than improve efficiency. Their separation in morphospace suggests broad-scale niche partitioning between members of these two clades, guided in part by phylogenetic constraint. Nonetheless, our patterns of shape and functional morphospace occupation show how both groups converged from basal amniote (faunivorous) morphologies28 towards a common amniote-specific form of herbivory29.At the level of FFGs, minimal overlap between the various therapsid and archosauromorph clades confirms that these herbivores were not in competition for most of the early Mesozoic, contrary to the competitive model (Fig. 3). When our FFGs are applied at ecosystem level for different localities (Fig. 4; Supplementary Data 11 and Supplementary Table 6), we find that most co-occurring taxa belonged to different FFGs. Examples of coexisting herbivores with the same feeding functionality (Supplementary Table 7), and thus possibly competing, include procolophonids, bauriids and rhynchosaurs in the Early Triassic, hyperodapedontine rhynchosaurs and dicynodonts in the Lower Ischigualasto Formation (Carnian), and within dinosaur-dominated assemblages of the latest Triassic and Early Jurassic (Fig. 3), which is expected as most of these dinosaur groups have been shown to employ similar ‘orthal’ jaw mechanics30. Widespread morphological dissimilarity suggests that high herbivore diversity in the Santa Maria, Ischigualasto, and Lossiemouth formations (Fig. 4) was sustained by niche partitioning, which enables ecologically similar taxa to coexist by diverging from each other in their demands on resources31,32. The subdivision of resources by specialisation towards separate niches minimises resource competition, whilst boosting feeding efficiency, and thus the chances of survival33,34,35.Fig. 4: Relative faunal abundances and potential competitive trophic conflicts within early Mesozoic assemblages through time.a The relative abundance of faunivores and herbivores. b The relative species richness of different therapsids and sauropsid clades. c The number of feeding functional group (FFG) conflicts in each assemblage. AZ Assemblage Zone, L Lower, No Number, Geological Events: CPE Carnian Pluvial Event, TJE Triassic-Jurassic mass extinction, Epochs: EJ Early Jurassic, ET Early Triassic, LT Late Triassic, MT Middle Triassic, Timebins: A Anisian, C Carnian, I Induan, L/C Ladinian/Carnian, N Norian, R Rhaetian, S Sinemurian, S/P Sinemurian/Pliensbachian, Diet: FnV Faunivores, HbV Herbivores, Taxonomic groups: BAm Basal Archosauromorpha, Ds Dinosauria, Pr Parareptilia, Psd Pseudosuchia, Sile Silesauridae, Th Therapsida.Full size imageOur FFGs are broadly defined, so even these examples of possible competition may be exaggerated. The further identification of large subgroups within the ingestion generalist FFG (Fig. 2) highlights this, as use of these subgroups dramatically reduced the occurrences of potential trophic conflict (Supplementary Data 11). Additionally, in the Carnian examples, the kannemeyeriiform dicynodonts were much larger36 and lacked the dental plates of rhynchosaurs37. These two clades may well have specialised on different plant food while coexisting within the same broad feeding guild. Further, among the Late Triassic herbivorous dinosaurs that also coexisted within broad feeding guilds (Fig. 3), niche partitioning has been noted already among sauropodomorph dinosaurs, expressed in their body size38 and postural disparity39. Further evidence of tetrapod niche differentiation may be found in their dentition40, body size41, limb anatomy42, and even spatiotemporal behaviour43. Therefore, other aspects of ecology may support divergent trophic strategies and the avoidance of competition within these groups, although further comparative studies are needed. Competition between Early Triassic diapsids is more convincing as there are greater levels of coexistence, similarities between sizes, and abundances where found together (Supplementary Data 10).Temporal trends: changing of the guildsPatterns of shape and functional disparity through geological time (Fig. 5a) generally show near reciprocal traces for therapsids and archosauromorphs—when values for one clade are trending upwards, those for the other are trending downwards. This is particularly apparent in the lower Carnian and Rhaetian. However, this pattern appears to vanish in the Norian, possibly due to poor sampling of the therapsids. Crossovers occur at the times of the Carnian Pluvial Event, 233 Ma, and in the aftermath of the Triassic-Jurassic mass extinction (TJE), 201 Ma. Both metrics broadly agree, showing rising archosauromorph shape and functional disparity through the Early and Middle Triassic, and then higher values for therapsids through most of the Late Triassic, and equivalent values in the Early Jurassic. Interestingly, this concordance breaks down in the Early Jurassic as a disconnect appears within therapsids (tritylodonts), with high shape disparity producing lower functional disparity.Fig. 5: The shape and functional disparity and morphospace occupation of early Mesozoic herbivores through time.a Shape (Procrustes variance) and functional (sum of variance) disparity of Archosauromorpha, Therapsida, and Parareptilia, with standard error bands. b Shape and functional morphospace time-slices at stage and substage levels. Major extrinsic, environmental events are shown by the dashed red line. Faunal turnovers are highlighted by stars. Misc Miscellaneous pseudosuchians, MPD Mean Pairwise distances, PTME Permo-Triassic mass extinction, CPE Carnian Pluvial Event, TJE Triassic-Jurassic extinction, Timebins: ANS Anisan, CHX Changhsingian, HET Hettangian, IND Induan. L, CRN Lower Carnian, L. NOR Lower Norian, LAD Ladinian, M. NOR Middle Norian, OLE Olenekian, PLB Pliensbachian, RHT Rhaetian, SIN Sinemurian, TOA Toarcian, U. NOR Upper Norian, WUC Wuchiapingian, All silhouettes created by S.S., but some are vectorised from artwork by Felipe Alves Elias (https://www.paleozoobr.com/) and Jeff Martz (United States National Park Service), available for academic use with attribution.Full size imageDividing the shape and functional morphospaces temporally as stacked plots shows more detail of how different herbivorous clades waxed and waned (Fig. 5b). Herbivore guilds in the Early Triassic were dominated by procolophonoids and dicynodonts. During the Middle Triassic, parareptile disparity rose as the Early Triassic disaster fauna was complemented by new groups such as the gomphodont cynognathian cynodonts and archosauromorph allokotosaurs and rhynchosaurs. Archosauromorph disparity also increased as diversity increased with the emergence of new groups with new forms and functions, such as the rhynchosaurs and allokotosaurs. Therapsid disparity remained stable with the diversification of many morphologically similar kannemeyeriform dicynodonts masking the new diversity of cynodonts.Near the beginning of the Late Triassic, the CPE marked a substantial change, as rhynchosaurs and dicynodonts disappeared or reduced to very low diversity and abundance, and archosauromorph herbivores took over11,12,13. These were initially aetosaurs and sauropodomorph dinosaurs and, while expanding in diversity, their disparity declined (Fig. 5a) because new taxa were morphologically conservative, exhibiting limited variance and emerging within the existing morphospace of each respective clade (Fig. 5b). At the same time, all other herbivore clades declined, with remaining (parareptile and dicynodont) taxa shifting towards the extreme edges of their former morphospace occupancy. Cynognathians also dwindled in the early Norian. This transition within the herbivore guilds marks a shift from oral to gut processing among the majority of large terrestrial herbivores23 (Figs. 2, 3, and 5b).During the Rhaetian, herbivore diversity and disparity declined with only dinosaur and mammalian herbivores surviving into the Jurassic. Both groups underwent morphological and taxonomic radiations in the Early Jurassic, with dinosaurs and mammals typically occupying the roles of large and small herbivores, respectively. There was also a brief reappearance of pseudosuchian herbivores. We note that through the course of the early Mesozoic, sauropsid and therapsid morphospace became increasingly distanced from each other, with further comparison of the distances between therapsid and archosauromorph morphospace centroids showing that this separation accelerated at the onset of the Late Triassic (Supplementary Table 12).At epoch scale, NPMANOVA identified significant shifts in morphospace occupation between the Early and Middle Triassic (shape and function: p = 0.02). At stage level, only the Olenekian-Anisian transition shows a significant shift in both shape and functional morphological diversity (shape: p = 0.009, function: p = 0.007) (Supplementary Table S14). These results denote the distinct shift from disaster faunas through the Early Triassic, marked by repeated climate perturbations, to the more stable conditions of the mid-Anisian onwards and faunal recovery from the PTME44,45. The transitions between the lower Carnian-upper Carnian and Sinemurian-Pliensbachian were identified as being significant to shape but not function (p = 0.01 and 0.03) (Supplementary Table 14). These results for the Carnian are tantalising and tentatively highlight the impacts of the CPE as an important macroevolutionary event13. Furthermore, at the p More
