Macroevolutionary ecomorphology of the Carnivora skull: adaptations and constraints in the extant species

Abstract

The mammalian order Carnivora is characterized by a broad taxonomic and ecological diversity. By using a large sample of extant species, we tested the impact of ecological factors on carnivoran skull (cranium and mandible) morphology, taking advantage of a combined geometric morphometrics and comparative method approach. We implemented several evolutionary models to account for different tempo and mode of evolution in size and shape data. These models validated the association between skull morphology and diet at the interspecific scale. The functional distinction between pinniped (aquatic) and fissiped (mostly terrestrial) taxa was found valid only in mandible shape and cranial size. High levels of morphological disparity and evolutionary rates were identified in specialized dietary groups, and positive association between rates and disparity was found for skull size. Cranium and mandible showed consistent patterns of covariation that reflect constrained functional processes, which stabilize the ecomorphological evolution of Carnivora. Aquatic adaptations allowed carnivorans to invade and persist within novel regions of the mandibular morphospace. This ecological shift did not increase morphological disparity but occurred at a faster rate than in terrestrial species. Those species exhibit a stronger level of cranio-mandibular covariation due to constraints imposed by more demanding masticatory adaptations.

Mandible shape variation and feeding biomechanics in minks

“…Alternatively, ecomorphology studies use an animal’s anatomy to infer its ecology (e.g. diet 16 ), which allows us to understand both what prey items an animal is capable of consuming and why, instead of observing what is it eating at a precise point in time.…”

“…Additionally, mandible morphology has been shown to be evolutionarily more plastic, reflecting dietary adaptations more accurately than the cranium, whose morphological evolution must respond to conflicting functional demands 23 – 25 . However, in the last decades, the consolidation of geometric morphometric methods has resulted in an increase in this type of study, which have revealed that mandible shape (i.e., all its geometric features except for size, position, and orientation) in carnivorans is not only related to function (i.e., mastication), but to a complex interaction of factors such as evolutionary history, body size, sexual dimorphism, diet and, in carnivorous species, prey size 16 , 23 , 26 – 31 .…”

“…We are aware that two-species studies are not adequate to define adaptations to environmental factors such as diet (see 39 ). Thus, dietary adaptations identified in multispecies studies on Carnivora 16 – 24 , 26 – 29 are used here as indicators of dietary capabilities.…”

Better sturdy or slender? Eurasian otter skull plasticity in response to feeding ecology

“…Its diet includes mainly fish, but also crustaceans, amphibians, reptiles, and, to a lesser extent, birds and mammals [ 23 – 27 ]. This high feeding plasticity is expected to be reflected in the cranial and mandibular morphology with modifications expected, especially in the dentition and masticatory muscle attachment area, as observed for members of the order Carnivora [ 21 , 28 ]. Furthermore, differences in diet may also be reflected in sexual dimorphism of the skull with respect to size and shape [ 29 – 32 ], as specific adaptations can improve the fitness and reduce intraspecific resource competition [ 33 ].…”

“…The skull is a complex anatomical adaptive structure, enclosing the central nervous system and the specialized sense organs and hosting the teeth used to capture, kill the prey, process and manipulate food [16]. Several studies have shown that in mammals, skull shape is closely related to diet [17][18][19][20][21], and shape changes in response to feeding habits can occur among different populations of the same species [22]. The Eurasian otter is an opportunistic feeder able to exploit different aquatic prey depending on their availability and catchability [23].…”