Jaw shape and mechanical advantage are indicative of diet in Mesozoic mammals

Jaw shape variation and diet in small mammals

Using 2D geometric morphometrics (Fig. 2a), we found that jaw shape is a good proxy for diet among small extant mammals. In Fig. 3, taxa with negative PC1 scores have shorter jaws, and taxa with positive PC1 scores have longer jaws; taxa with positive PC2 scores have taller ascending rami and taxa with negative PC2 scores have shorter ascending rami. Among extant mammals, most dietary categories (excluding omnivores) can be distinguished along PC1 (Fig. 3a): herbivores plot at the negative end of PC1, insectivores towards the positive end, and carnivores in between. These categories are also statistically different from each other (Table 2), showing that jaw shape can distinguish between most major dietary types. However, our data cannot distinguish between carnivores and omnivores.

Data on the jaw shape of Mesozoic mammals were projected onto the extant taxa morphospace (Fig. 3b). In order to determine whether jaw shape could be used as a dietary proxy in Mesozoic mammals, we obtained previous independent determinations of likely diets, which variously employed dental morphology, tooth wear facets and body size (e.g., see refs. ^{1,7,12,14,24,25,26,27,28,29,30,31,32}). We saw a very good correspondence between previous proposed diets for Mesozoic mammals and their position on the morphospace. See Supplementary Fig. 6 for a principal components analysis scatter plot which includes multituberculates and haramiyidans; these taxa were excluded from our study because the vast majority of them have jaw shapes dissimilar to the other extinct and extant mammals in our sample (i.e., allotherians have shorter jaws and thus more negative PC1 scores).

Stem mammals

Most stem mammals plot within the morphospace of extant insectivores and have positive PC1 scores. One exception is Sinoconodon (taxon #2, Fig. 3), which plots within the morphospace of extant carnivores; Sinoconodon is considered a carnivore based on dental morphology⁵. Haramiyavia (#1) is thought to have been a plant-dominated omnivore²³ based on dental morphology, but here it plots within the morphospace of extant insectivores. Both morganucodontans in this study, Morganucodon (#3) and Dinnetherium (#4), have similar PC1 scores to extant insectivores, echoing the findings of Gill et al.¹⁴.

Molar morphology indicates omnivorous or faunivorous diets for docodontans; here they mostly plot within the morphospace of extant insectivores, with the exception of Haldanodon (#6) and Docofossor (#7). Agilodocodon (#9) was previously considered a plant-dominated omnivore, with exudativorous dental features which indicated a diet mainly composed of plant sap³³; more recently, Wible and Burrows³⁴ challenged this hypothesis and suggested that the teeth of Agilodocodon most closely resemble those of extant insectivores. Here, Agilodocodon plots firmly within the morphospace of extant insectivores, close to the insectivorous dusky antechinus (Antechinus swainsonii, #61) and the elephant shrews (Elephantulus rufescens [#114] and E. brachyrhynchus [#115]), which are insect-dominated omnivores.

According to Ji et al.²⁸ the swimming docodontan, Castorocauda (#5), has dental features indicative of feeding on aquatic invertebrates and small vertebrates, like fish. Castorocauda is often depicted as being carnivorous and, particularly, piscivorous^7,28,33. The jaw shape of Castorocauda is similar to that of modern day insectivores; this docodontan might have been feeding on “soft” aquatic invertebrates (Fig. 3). The other Mesozoic mammal in our sample proposed to have been semi-aquatic, Teinolophos (#13), plots in a similar area of the morphospace to Castorocauda. Our extant sample also includes a semi-aquatic carnivore, the water opossum (Chironectes minimus, #69), which plots in the middle of the carnivore morphospace, far away from Castorocauda and Teinolophos.

Docofossor (#7) has skeletal features indicative of a fossorial lifestyle and a dentition similar to those of extant mammals foraging underground, such as moles, solenodons, and tenrecs³⁵. This docodontan has previously been considered an insectivore⁷. Here, Docofossor plots within the morphospace of extant carnivores; however, it plots close to the burrowing Hispaniolan solenodon (Solenodon paradoxus, #109), which has an insectivorous diet. Among the extant insectivores in our sample, the burrowing vermivores (e.g., the hairy-tailed mole, Parascalops breweri [#108], and the Hispaniolan solenodon) have more negative PC1 scores than other insectivores (similar to that of Docofossor), and their PC1 values are more similar to those of carnivores.

The dental morphology of Haldanodon (#6) is indicative of an insectivorous diet. Here, it plots within the carnivore morphospace (very near extant herbivores), because of its tall coronoid process and comparatively shorter jaw. Docodon (#8) likely ate insects and other small invertebrates²⁷ and, based on its diminutive size³⁶, Microdocodon (#10) was probably insectivorous. Both of these docodontans plot within the insectivore morphospace.

Non-therian crown mammals

The jaw shape of non-therian crown mammals varies widely, plotting mostly within the morphospace of insectivores and carnivores. Fruitafossor (#11), a fossorial mammal with teeth similar to extant armadillos, has been considered an omnivore eating insects, small invertebrates and some plants²⁶. Here, it plots within the insectivore morphospace, closely to the insectivorous and fossorial hairy-tailed mole (Parascalops breweri, #108), and shares similar PC1 scores with other fossorial taxa, such as Docofossor (#7) and the Hispaniolan solenodon (#109).

Extant monotremes eat insects and other small invertebrates. It has been proposed that the Early Cretaceous monotreme Teinolophos (#13) had a semiaquatic lifestyle (on the basis of its enlarged mandibular canal³⁷) and ate in a similar manner to the insectivorous Kuehneotherium³⁸. Here Teinolophos, and the australosphenidan Henosferus (#12), have PC1 scores similar to insectivores and omnivores.

The eutriconodontans are a very diverse group of insectivores and carnivores which had a wide range of body sizes, including some of the largest Mesozoic mammals known¹. Here all eutriconodontans fall within or very close to the extant carnivore morphospace. In particular, Triconodon (#16) and Argentoconodon (#19) plot within the carnivore morphospace, Trioracodon (#17) and Volaticotherium (#18) plot between the carnivore and insectivore morphospaces, and Yanoconodon (#15) plots within the insectivore morphospace. Both gobiconodontids, Gobiconodon (#20) and Repenomamus (#21), have more negative PC1 scores and plot closer to the herbivore morphospace, but still remain within or close to the carnivore morphospace. Triconodon, Trioracodon, Gobiconodon, and Repenomamus are all considered carnivores based on craniodental morphology and body size^1,7,31; additionally, there is direct evidence for the carnivorous diet of Repenomamus from fossilized stomach contents⁴. Yanoconodon and Volaticotherium are considered insectivores⁷.

“Symmetrodontans” like Spalacotherium (#22), Zhangheotherium (#24) and Maotherium (#25) have often been considered insectivores based on their craniodental morphology^1,7 (note “symmetrodontans” likely do not represent a monophyletic group, but are often grouped together based on their tooth morphology¹). Here, all “symmetrodontans” plot within the insectivore morphospace. Dryolestids are also commonly considered insectivorous^1,29. Here, Crusafontia (#26) plots between the morphospace of extant carnivores and insectivores, while Amblotherium (#27) plots within the insectivore morphospace.

Vincelestes (#29) has previously been considered a carnivore on the basis of jaw shape¹². Here, it plots near the morphospaces of both omnivores and herbivores. Bonaparte²⁴ considered the incisor wear of Vincelestes reminiscent of Cenozoic carnivores, and Rougier²⁵ considered its jaw morphology indicative of a forceful bite enabling the incorporation of tough plant matter into a primarily carnivorous/insectivorous diet.

Therian crown mammals

Extant marsupials have a large diversity of diets, including herbivory, but the extinct metatherians in our sample are considered to have been limited in diet to insectivory and carnivory (note that there are some putatively herbivorous/omnivorous extinct metatherians, like Glasbius and polydolopimorphians^39,40). Their jaw shape is very similar to that of extant carnivores and insectivores (Fig. 3). Dental morphology indicates that Eodelphis (#32) and Deltatheridium (#30) were carnivorous, Didelphodon (#31) durophagous or molluscivorous^31,32, and Alphadon (#33) is considered to have been insectivorous, on the basis of its jaw shape and body size¹². Dental microwear indicates a broad diet consisting of vertebrates, plants, and hard-shelled invertebrates for Didelphodon; biomechanical analyses of its skull and jaw points towards a durophagous diet^15,16. Biomechanical analyses of the resistance to bending and torsion of Eodelphis jaws, points to a durophagous diet in Eodelphis cutleri and non-durophagous faunivory for Eodelphis browni¹⁶. Here, Eodelphis, Deltatheridium and Didelphodon plot closely to the extant carnivores, while Alphadon plots closely to the extant insectivores.

Extant placentals also have a wide range of diets, but many of the extinct eutherians in this study (i.e., Sinodelphys [#34], Juramaia [#35], Eomaia [#36], Kennalestes [#40], Barunlestes [#44], and Kulbeckia [#43]) are considered insectivorous^7,12. Here, we corroborate this hypothesis (Fig. 3): all extinct eutherians plot within the insectivore morphospace, with the exception of Asioryctes (#38) which plots in the insectivore/carnivore morphospace, and Juramaia and Sinodelphys, which plot just outside the insectivore morphospace.

Using jaw shape to infer diet in Mesozoic mammals

We performed a phylogenetic flexible discriminant analysis (phylo FDA) following Motani and Schmitz⁴¹ to determine the posterior probability of the Mesozoic taxa belonging to one of three dietary categories: insectivore, carnivore, or herbivore (we omitted omnivores as they are not well discriminated in Fig. 3). We used the first seven PC scores (of the PCA of Procrustes coordinates of jaw shape), which together accounted for 81.39% of the variance. The results of the analysis can be seen in Fig. 4 and the posterior probability values can be seen in Supplementary Data 1. We used the extant taxa of known diets as the training dataset for the discriminant analysis: these taxa were classified correctly 89.19% of the time. For the most part, we see a good separation between dietary groups among extant mammals (Fig. 4a), with some exceptions: the primarily herbivorous olingo (Bassaricyon gabbii, #94) plots with the carnivores (although mainly frugivorous, it can consume small vertebrates), and a couple of insectivores plot very near the carnivores (i.e., the little brown bat [Myotis lucifugus, #104] and the Hispaniolan solenodon [Solenodon paradoxus, #109]). These three taxa, alongside the carnivorous greater bulldog bat (Noctilio leporinus, #101), were the only extant taxa misclassified by the discriminant analysis.

The Mesozoic mammals included in our sample have largely been considered faunivorous and the results of the phylo FDA (Fig. 4b) corroborate this hypothesis. The majority of them are classified as insectivorous, including most stem mammals, australophenidans, “symmetrodontans” and eutherians, among others. Among the eutriconodontans, Argentoconodon, Gobiconodon, Repenomamus, and Trioracodon, are classified as carnivores, Triconodon and Yanoconodon are classified as insectivores, but with moderate support (posterior probabilities: 48% and 52%, respectively), and Phascolotherium and Volaticotherium are more confidently classified as insectivores (posterior probabilities: 60% and 73%, respectively). Among the metatherians, Didelphodon and Eodelphis are classified as carnivores, while Alphadon and Deltatheridium are classified as insectivores with moderate support (posterior probabilities: 54% and 52%, respectively). The stem mammals, Haramiyavia, Sinoconodon, and Docofossor are all confidently classified as carnivores (posterior probabilities over 80%), and the crown mammals Crusafontia and Kennalestes are also classified as carnivores, but with moderate support (posterior probabilities: 54% and 52%, respectively). Two taxa in the analysis are classified as herbivores, because of their relatively tall ascending rami: Vincelestes (#29) and Haldanodon (#6). The dental morphology of Vincelestes points to a primarily faunivorous diet²⁴, but it has been previously noted that its jaw morphology is indicative of a forceful bite; Rougier²⁵ suggested that this jaw morphology might have enabled Vincelestes to incorporate tough plant matter into its diet, but it might also be indicative of durophagy. The dental morphology²⁷ and body size of Haldanodon point towards an insectivorous diet; in this analysis, the posterior probability of Haldanodon being a herbivore is not high (only 40.3%). The evidence thus far suggests Haldanodon had a faunivorous diet; its jaw morphology might be indicative of the incorporation of tougher food sources into its diet.

Mechanical advantage of the jaws of small mammals

We obtained mechanical advantage (MA) data to test whether extant mammals of different dietary groups have distinct MA values (Table 3). The mechanical advantage measurements were standardized across all jaws to account for differences in jaw morphology (e.g., presence or absence of the angular process) (Fig. 2b); the outlever was measured at the anterior end of the jaw and at the first lower molar (m1). When measuring mechanical advantage at the jaw tip and considering extant taxa only, we find statistically significant differences in the mechanical advantage of the masseter (MAM) values in all pairwise dietary combinations except for carnivore-insectivore (Table 3). The mechanical advantage of the temporalis (MAT) is statistically distinct only between herbivores and insectivores, and carnivores and insectivores (Table 3). Herbivores and carnivores do not have statistically distinct MAT values. This may differ in a sample of larger (> 5 kg) therians. When measuring the outlever at the m1, we find statistically significant differences in all pairwise comparisons of MAM between dietary groups, except for herbivore–omnivore and carnivore–insectivore. When considering MAT, we only find significant differences between omnivores and carnivores, insectivores and herbivores, and insectivores and carnivores.

Figure 5 shows the mechanical advantage of the masseter (left) and temporalis (right), measured at the jaw tip, in a phylogenetic context (see also Supplementary Fig. 7 for individual taxon names). Phylogeny appears to have a large influence on the mechanical advantage and diet of the jaws of small mammals. Most Mesozoic taxa have low (blue) to intermediate (green) MAM values. Most stem mammals have intermediate (green) to high (red) MAM values and non-therian crown mammals have low MAM values, with the exception of Fruitafossor and Vincelestes (the latter has the highest MAM value of all taxa, both extinct and extant). Most eutherians, both extinct and extant, have intermediate to low MAM values, with the exception of the relatively high values (yellow to orange) seen in elephant shrews (order Macroscelidea) and the four-toed hedgehog (order Eulipotyphla, Atelerix albiventris). Some members of the orders Carnivora (including canids and euplerids) and Afrosoricida have some of the lowest MAM values. Metatherians have MAM values ranging from low to intermediate (in the orders Dasyuromorphia and Didelphimorphia, as well as in the Mesozoic metatherians) to some of the highest in the order Diprotodontia (e.g., the sugar glider [Petaurus breviceps], the woylie [Bettongia penicillata], the cuscus [Phalanger orientalis]).

Most taxa have intermediate MAT values (Fig. 5 and Supplementary Fig. 7). Very low MAT values are seen in the extinct non-therian crown mammals Teinolophos and Zhangheotherium and a few extant taxa, including marsupials like the Western barred bandicoot (Perameles bougainville) and the numbat (Myrmecobius fasciatus), and placentals such as the striped treeshrew (Tupaia dorsalis) and the short-snouted elephant shrew (Elephantulus brachyrhynchus). The highest MAT values belong to members of the order Carnivora, including skunks (Mephitis macroura and Conepatus humboldtii), the least weasel (Mustela nivalis) and the tayra (Eira barbara). Some diprotodontians like the common ringtail possum (Pseudocheirus peregrinus) and the sugar glider (Petaurus breviceps) also have relatively high MAT values. Some extinct taxa also have relatively high MAT values, including the stem mammal Docofossor, and the non-therian crown mammals, Triconodon and Vincelestes.

Figures 6 and 7 present a visualisation of the mechanical advantage of the masseter and the temporalis (x axis, outlever measured at the jaw tip) and the PC1 scores of Fig. 3 (y axis, mainly describes jaw length) because, as previously mentioned, this is the axis in which dietary categories among extant mammals are best discriminated. In the y axis of Figs. 6a and 7a, herbivores have short jaws, carnivores have short to intermediate-length jaws and insectivores have intermediate-length to long jaws. In Fig. 6a, insectivores and carnivores have low mechanical advantage values of the masseter (i.e., when biting: less forcefulness, more speed), and herbivores have higher mechanical advantage values (i.e., when biting: more forcefulness, less speed). In Fig. 7a, insectivores have lower mechanical advantage values of the temporalis, while carnivores and herbivores have higher mechanical advantage values. Note that most carnivores have intermediate MAT values, but some mustelids (i.e., the least weasel [Mustela nivalis, #99], the American badger [Taxidea taxus, #96], and the North American river otter [Lontra canadensis, #98]), have the highest MAT values among extant mammals. Also note that, among insectivores, those with the highest MAT values are burrowing vermivores (i.e., the short-tailed shrew tenrec [Microgale brevicaudata, #111], the hairy-tailed mole [Parascalops breweri, #108], and the Hispaniolan solenodon [Solenodon paradoxus, #109]). By using a combination of their MAM and MAT values (as well as their jaw length), we can distinguish dietary categories among extant mammals. We decided to omit omnivores from these figures because, as seen in Fig. 3, they cannot be distinguished from other dietary groups on the basis of jaw shape.

We also obtained additional mechanical advantage measurements, in which the outlever was measured at the first lower molar (m1), rather than the jaw tip (Supplementary Figs. 8, 10, 11, and 13). We made this alternative measurement because Grossnickle¹⁷ found that the length of the posterior portion of the jaw (measured from the jaw joint to the m1) is a strong predictor of diet in mammals. Compared to the mechanical advantage (MA) measurements at the jaw tip (Figs. 6a and 7a), we see a less clear distinction between dietary groups among extant mammals. There is considerable overlap between dietary groups in Supplementary Fig. 10 (jaw length~MAM). In Supplementary Fig. 11 (jaw length~MAT), there is a better separation between dietary groups.

Based on previous likely determinations of diet of Mesozoic mammals (see Supplementary Data 1 for the full list of sources), most taxa plot where it is “expected” of them, with some exceptions (Figs. 6b and 7b): 1) about half of the stem mammals (i.e., Haramiyavia, Sinoconodon, Morganucodon, Haldanodon, and Docofossor), most of which are thought to have been faunivorous, have higher MAM values than modern insectivores and carnivores, and 2) the docodontan Castorocauda has MAM and MAT values consistent with an insectivorous diet, as opposed to the carnivorous diet proposed for this taxon^7,28,33. Most Mesozoic mammals have mechanical advantage values similar to modern insectivores, a few taxa are similar to carnivores (e.g., Sinoconodon, Triconodon, Trioracodon, Argentoconodon, Gobiconodon, Repenomamus, Deltatheridium, Didelphodon, and Eodelphis), and some are more similar to herbivores (e.g., Vincelestes and Fruitafossor).

Source: Ecology - nature.com