Masticatory muscle architecture in a water‐rat from Australasia (Murinae, Hydromys) and its implication for the evolution of carnivory in rodents

Abstract

Murines are well known for their generalist diet, but several of them display specializations towards a carnivorous diet such as the amphibious Indo-Pacific water-rats. Despite the fact that carnivory evolved repeatedly in this group, few studies have investigated associated changes in jaw muscle anatomy and biomechanics. Here, we describe the jaw muscles and cranial anatomy of a carnivorous water-rat, Hydromys chrysogaster. The architecture of the jaw musculature of six specimens captured both on Obi and Papua were studied and described using dissections. We identified the origin and insertions of the jaw muscles, and quantified muscle mass, fiber length, physiological cross-sectional area, and muscle vectors for each muscle. Using a biomechanical model, we estimated maximum incisor and molar bite force at different gape angles. Finally, we conducted a 2D geometric morphometric analyses to compare jaw shape, mechanical potential, and diversity in lever-arm ratios for a set of 238 specimens, representative of Australo-Papuan carnivorous and omnivorous murids. Our study reveals major changes in the muscle proportions among Hydromys and its omnivorous close relative, Melomys. Hydromys was found to have large superficial masseter and temporalis muscles as well as a reduced deep masseter and zygomatico-mandibularis, highlighting major functional divergence among omnivorous and carnivorous murines. Changes in these muscles are also accompanied by changes in jaw shape and the lines of action of the muscles. A more vertically oriented masseter, reduced masseteric muscles, as well as an elongated jaw with proodont lower incisors are key features indicative of a reduced propalinality in carnivorous Hydromys. Differences in the fiber length of the masseteric muscles were also detected between Hydromys and Melomys, which highlight potential adaptations to a wide gape in Hydromys, allowing it to prey on larger animals. Using a biomechanical model, we inferred a greater bite force in Hydromys than in Melomys, implying a functional shift between omnivory and carnivory. However, Melomys has an unexpected greater bite force at large gape compared with Hydromys. Compared with omnivorous Melomys, Hydromys have a very distinctive low mandible with a well-developed coronoid process, and a reduced angular process that projects posteriorly to the ascending rami. This jaw shape, along with our mechanical potential and jaw lever ratio estimates, suggests that Hydromys has a faster jaw closing at the incisor, with a higher bite force at the level of the molars. The narrowing of the Hydromys jaw explains this higher lever advantage at the molars, which constitutes a good compromise between a wide gape, a reduced anterior masseteric mass, and long fiber lengths. Lever arms of the superficial and deep masseter are less favourable to force output of the mandible in Hydromys but more favourable to speed. Compared with the small input lever arm defined between the condyle and the angular process, the relatively longer mandible of Hydromys incr...

Australian rodents reveal conserved Cranial Evolutionary Allometry across 10 million years of murid evolution

“…Folivores showed higher PC2 values corresponding to broader molars than non-folivorous species of the same size. Carnivores showed lower PC2 scores, with fewer teeth and a rostrum morphology adaptive for capturing prey; an unusual niche for rodents (Fabre et al 2017). These morphological changes did not alter the conserved species-level allometric slope, even for carnivorous water rat, Hydromys chrysogaster, whose mean projected shape to size ratio falls noticeably above the common evolutionary allometric trajectory.…”

Divergent in shape and convergent in function: Adaptive evolution of the mandible in Sub-Antarctic mice

“…Yet, species specializing toward carnivory or insectivory display‐specific adaptations that modulate this generalist morphology (Samuels ; Fabre et al. ). The case of the Sub‐Antarctic mice suggests that such fine‐tuning may occur even at the intraspecific level.…”

“…In contrast, the superficial masseter/incisor MA is decreased. Increased action of the temporalis and decreased contribution of the masseter have been described in carnivorous murine rodents (Fabre et al 2017). They may contribute, together with the increased incisor out-lever arm, to an action favoring speed instead of force at incisor biting.…”

“…The mandible of omnivorous murine rodents is known as a paradigm example of a versatile generalist tool adapted to all feeding modes (Cox et al 2012). Yet, species specializing toward carnivory or insectivory display-specific adaptations that modulate this generalist morphology (Samuels 2009;Fabre et al 2017). The case of the Sub-Antarctic mice suggests that such fine-tuning may occur even at the intraspecific level.…”

The Ontogeny of Masticatory Muscle Architecture in Microcebus murinus

“…The arrangement of muscle fascicles within the masticatory apparatus has been shown to correlate with dietary adaptations in both primates (Perry and Wall, ; Eng et al, ; Taylor and Vinyard, ; Perry and Hartstone‐Rose, ; Perry et al, ; Perry et al, ; Hartstone‐Rose et al, ) and other mammals (Taylor et al, ; Herrel et al, ; Hartstone‐Rose et al, ; Santana and Cheung, ; Fabre et al, ; Curtis and Santana, ; Santana, ). Despite our understanding of the relationship between fascicular architecture and masticatory function, however, few studies have considered how this architecture changes throughout the lifetime of an animal (Huhov et al, ; Langenbach and Weijs, ; Pfaller et al, ; Pfaller et al, ), especially within the primate order (though see Dickinson et al, ).…”