Niche partitioning shaped herbivore macroevolution through the early Mesozoic

Triassic herbivore ecomorphological feeding guilds

We 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 Triassic^14,16,21.

Contour 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).

Niche partitioning and competition avoidance

Were 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 resources^31,32. The subdivision of resources by specialisation towards separate niches minimises resource competition, whilst boosting feeding efficiency, and thus the chances of survival^33,34,35.

Our 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 guilds

Patterns 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.

Dividing 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 over^11,12,13. 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 PTME^44,45. 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 < 0.1 significance level, the functional differences between these two transitions are recovered as significant (p = 0.06 and 0.05), as well as the Pliensbachian-Toarcian transition (p = 0.1). However, it must be noted that if a Bonferroni correction is applied, we are unable to recover any significant results for stage transitions.

We recognise a repeated pattern in the replacements in herbivore guilds that coincided with the three crisis events: (1) In the case of the PTME, so many clades had been entirely wiped out by the severity of the extinction that the few species of procolophonoids and dicynodonts that survived^2,46 would likely have occupied a much reduced ecospace relative to the latest Permian. While procolophonoids began to decline in the Anisian, dicynodonts radiated alongside new rhynchosaurs and cynognathians. These clades came to dominate Middle Triassic herbivore guilds. (2) The CPE hit these dominant groups hard, with survivors hanging on in the peripheries of their former morphological and functional space (Fig. 5b). Through the Norian and Rhaetian, these taxa became further confined to extreme areas of morphospace, whilst new archosaurian herbivores radiated. (3) The TJE was a major blow for the last procolophonoids, dicynodonts and cynognathians, (rhynchosaurs having already succumbed to extinction in the early Norian), as well as the aetosaurs, which had been important elements within Norian faunas (Fig. 3c). We find that these taxa actually began to decline during the Norian (Fig. 5). The decline in these formerly dominant groups is mirrored by expansion of new dinosaur and mammalian herbivore clades. Despite also suffering through the latest Triassic, both groups radiated in the Early Jurassic, moving into space vacated by aetosaurs and cynognathians, respectively. The Early Jurassic fossil record is limited, but total herbivore shape and function space were later refilled by sauropodomorph and ornithischian dinosaurs, as well as new mammalian clades.

This pattern of marginalisation seen in both shape and function space (Fig. 5b) documents how stressed clades apparently ‘retreat’ into specialised niches at the periphery of their former occupancy. Sampling issues may confound observation of this pattern at stage level, but epoch-level comparisons of morphospace occupation highlights this pattern of declining disparity in certain clades through the Triassic (Fig. 6). This is seen three times through the Triassic and Early Jurassic, as the last parareptiles, rhynchosaurs and dicynodonts were pushed to peripheral positions in shape and function space after the rigours of the three mass extinction events (PTME, CPE, TJE). Likely then, the last survivors of each of these clades had become trophic specialists. As specialists, dicynodonts, hyperodapedontine rhynchosaurs and leptopleuronine procolophonids were potentially more constrained than the new archosaur herbivores in shifting their diets towards the new prevailing flora. Survivors became further entrenched within specialist niches and rare following the crises. In becoming highly specialised, these groups were forced along an evolutionary ratchet⁴⁷ that amplified extinction risk as the environment changed and those niches disappeared. Specialists may outcompete generalists where high quality resources are readily available and stable⁴⁸.

Consequently, this trophic specialism in combination with reduced abundance suggests this ‘ecological entrenchment’ is possibly correlated with geographic retrenchment to where preferred resources remained abundant, with the reduction in numbers and geographic spread exacerbating extinction risk^49,50. ‘Marginal’ morphospace occupation may be followed by further restriction of MO to a smaller subset of morphospace (Figs. 5b and 6), which may relate to further ‘hyper-specialisation’ or perhaps the ongoing loss of refugia as conditions became increasingly adverse. Nonetheless, poor sampling is an acute issue, particularly as these clades approached extinction in the Late Triassic, so further study is required to test these tentative interpretations. Ecological entrenchment may have served to minimise competitive pressures and prolong survival in the face of increasingly heterogenous environmental conditions and new competitors that were able to better exploit predominant plant resources.

Extrinsic controls on herbivore macroevolution

Triassic climates oscillated between acute humid and extended dry phases⁵¹, and these fluctuations triggered widespread and significant remodelling of terrestrial floras^5,52. Floral turnovers coincided with pulses of change in herbivore guilds. The transition from palaeophytic to mesophytic plant assemblages through the Ladinian and Carnian⁵² coincided with reduced morphospace packing by non-archosaurian herbivores (Figs. 3c and 5b). Herbivore functional diversity among dinosaurs and pseudosuchians expanded following the CPE. Widespread wetter climates in the CPE^53,54 may have triggered radiations of Bennettitales, Gnetales, and modern ferns and conifers⁵, associated with the expansion of archosaurian herbivore diversity and taxon density within archosaur morphospace, which counter-intuitively reduced archosaur disparity (Fig. 5a). Increased morphospace packing by archosaurian herbivores (Fig. 5b) tentatively suggests that the increased prominence of some gymnosperms as arid conditions returned in the Norian⁵² may be linked to the survival of archosaur herbivores, particularly sauropodomorphs through the Carnian-Norian transition, whilst other herbivore groups perished.

The CPE was critical in triggering the decisive switch from dominance by therapsids as herbivores to the real beginning of the ‘age of dinosaurs’ (Figs. 3, 4, and 5). Before the CPE, rhynchosaurs and dicynodonts comprised 50–80% of individuals within well sampled faunas, whereas after the CPE they had dwindled to low abundance, and aetosaurs and sauropodomorph dinosaurs replaced them numerically, in some Norian faunas comprising 80–90% of individuals¹³. The TJE saw the end of aetosaurs, but sauropodomorphs continued to diversify and retained their ecological dominance as large herbivores, alongside the newly diversifying ornithischian dinosaurs.

The CPE did not cause the extinction of rhynchosaurs and dicynodonts but made them rare (Figs. 3 and 4). Rhynchosaurs went extinct in the early Norian⁵⁵, whereas dicynodonts survived to the end of the Triassic, but at reduced diversity, abundance, and disparity^56,57. This example shows the value of metrics of ecological abundance rather than species richness. Dicynodonts survived within wetter environments, even within dinosaur-dominated ecosystems⁵⁸. Some of these latest taxa, such as Lisowicia bojani in Poland, even achieved huge body sizes that rivalled those of contemporaneous large sauropodomorphs^19,59. The survival of kannemeyeriform dicynodonts might be because their typically large body sizes enabled them to explore wider geographic areas in search of suitable habitats. Nonetheless, they succumbed before the end of the Triassic alongside aetosaurs and cynognathian cynodonts⁴ (Fig. 3c). The end-Triassic saw widespread deforestation alongside a dramatic reorganisation of global floras that favoured ferns, at the expense of tropical flora^60,61. Sparse floras dominated by ferns would have served as a poor food resource for large herbivores⁶² and therefore may be linked to the extinction of the aforementioned herbivore clades, which were largely low- to mid-level browsers.

We find that the largest episodes of morphospace expansion occur during the supposed recovery intervals of mass extinction events, with some surviving clades (particularly dinosaurs) showing much greater MO than before the extinction event (Fig. 5b). Morphospace expansion following the PTME occurs relatively quickly compared to the TJE, suggesting a relatively faster ecological recovery. Following the PTME and the loss of most species, total herbivore disparity and FFGs reached maximum levels in the Anisian, whereas following the TJE, the rebound in morphological diversity was modest, even by the end of the Early Jurassic. However, there is an edge effect here as we have not continued the analysis into the Middle Jurassic, and there may be sampling problems, as there are few well documented terrestrial tetrapod faunas in the Sinemurian and Pliensbachian. The inclusion of later dinosaur taxa and the overall diversification of dinosaurs in the Jurassic would likely yield a greater diversity of FFG in the later Jurassic than seen at the end of the Early Jurassic.

Furthermore, it is likely that the FFGs (light oral processors, shearing pulpers, and durophagous specialists) that disappeared within the Triassic would re-emerge as the climatic conditions stabilised from the end-Triassic event and terrestrial floras recovered^52,54; the resurgence of floral diversity would likely have spurred new herbivorous diversification in both dinosaurs and mammals. The lost and depleted guilds identified here were likely restored as new dinosaurian and mammalian herbivores evolved through the later Mesozoic. Previous work highlights the prevalence of convergent evolution within dinosaurs²⁴, and this is recognised here with repeated patterns of specialisation towards higher biting efficiency and greater oral processing in procolophonoids, rhynchosaurs, aetosaurs and ornithischians (Figs. 1 and 2). The prevalence of these patterns across quite phylogenetically distant clades emphasises that ecomorphs can disappear and reappear as conditions permit. This is further illustrated by the continuation of the prehension specialist FFG through the TJE with minimal change (Fig. 3b), despite the loss of its main constituent clade, the aetosaurs. The extinction of the aetosaurs in the TJE was offset by the emergence of heterodontosaurid ornithischians and likely later thyreophorans as the Jurassic progressed and they followed the common ‘herbivore adaptive pathway’ (Figs. 2 and 3c). Aetosaur-thyreophoran convergent evolution was not limited to jaw mechanics as ankylosaurs evolved similar armoured morphologies, and ecologies as large, quadrupedal, low-level feeders. However, these later thyreophorans developed more complex and powerful jaw mechanics³⁰, allowing them to diverge from aetosaurs and exploit different niches as specialised herbivores.

Our study shows substantial ecological shifts occurred mostly at times of environmental instability, with only incremental development of ecospace during times of relative stability. This highlights a fluctuation between times of normal or ‘Red Queen’ evolution typified by adaptation to intrinsic pressures, punctuated by times of crisis or ‘Court Jester’ evolution, when large-scale extrinsic events provide the dominant selective pressures⁷. Our results confirm recent findings using model-based analyses that intrinsic, competitive interactions are the key to maintaining stasis within community assemblages through deep time^48,63. Stasis is the norm, characterised by relatively stable climates and floras and honing of the adaptations of herbivores and slow expansion of morphospace occupation through biotic interaction. The environmental perturbations of the three global crises, all involving sharp global warming, extremes of humidity and aridity, and acid rain nearly but not quite killed off the dominant incumbent herbivores. The few survivors endured at the periphery of their former shape and function spaces, perhaps ecologically marginalised due to loss of food sources or because other surviving herbivores monopolised the newly prevalent vegetation. Episodes of instability mark a flip from dominance of competitive ability as the key driver of evolution to opportunism in perturbed times when the winners and losers might reflect entirely different selective advantages.

Source: Ecology - nature.com