Biting through constraints: cranial morphology, disparity and convergence across living and fossil carnivorous mammals

Abstract

Carnivory has evolved independently several times in eutherian (including placental) and metatherian (including marsupial) mammals. We used geometric morphometrics to assess convergences associated with the evolution of carnivory across a broad suite of mammals, including the eutherian clades Carnivora and Creodonta and the metatherian clades Thylacoleonidae, Dasyuromorphia, Didelphidae and Borhyaenoidea. We further quantified cranial disparity across eutherians and metatherians to test the hypothesis that the marsupial mode of reproduction has constrained their morphological evolution. This study, to our knowledge the first to extensively sample pre-Pleistocene taxa, analysed 30 three-dimensional landmarks, focused mainly on the facial region, which were digitized on 130 specimens, including 36 fossil taxa. Data were analysed with principal components (PC) analysis, and three measures of disparity were compared between eutherians and metatherians. PC1 showed a shift from short to long faces and seemed to represent diet and ecology. PC2 was dominated by the unique features of sabre-toothed forms: dramatic expansion of the maxilla at the expense of the frontal bones. PC3, in combination with PC1, distinguished metatherians and eutherians. Metatherians, despite common comparisons with felids, were more similar to caniforms, which was unexpected for taxa such as the sabre-toothed marsupial Thylacosmilus. Contrary to previous studies, metatherian carnivores consistently exhibited disparity which exceeded that of the much more speciose eutherian carnivore radiations, refuting the hypothesis that developmental constraints have limited the morphological evolution of the marsupial cranium.

Figure 1.

Landmarks captured on each specimen, shown here on Didelphis virginiana (Adapted from [24]). Landmarks are detailed in the electronic supplementary material, table S1.

Figure 2.

PC analyses. (a) PCs1 and 2. Metatherians are represented by letters, and eutherians by symbols, as detailed. Open symbols represent extinct taxa, and closed symbols denote extant taxa. Wireframe models of cranial shapes at the end of each axis are shown in dorsal view. PC1 represents a shift from short-faced, generally hypercarnivorous forms on the negative end to long-faced insectivorous forms on the positive end. Metatherians are concentrated on the positive end of PC1, and felids define the negative end. The positive extreme of PC2 is defined by the isolated sabre-toothed metatherian, Thylacosmilus atrox, with sabre-toothed felids (open yellow cats) falling in an intermediate region between Thylacosmilus and all other sampled taxa. Interestingly, the third group of sabre-toothed carnivores, nimravids (multicoloured cats) fall with the rest of carnivores, rather than with other sabre-toothed forms on PC2. Overlap is strongest between caniforms and metatherians. (b) PCs1 and 3, with wireframe models shown for the extremes of PC3. There is clearer separation between metatherians and eutherians in this graph. Creodonts (multicoloured circles) fall between most metatherians and eutherians, though caniforms again overlap with some metatherians.