Since their arrival approximately 200 years ago, the house mice (Mus musculus) on Gough Island (GI) rapidly increased in size to become the largest wild house mice on record. Along with this extreme increase in body size, GI mice adopted a predatory diet, consuming significant quantities of seabird chicks and eggs. We studied this natural experiment to determine how evolution of extreme size and a novel diet impacted masticatory apparatus performance and functional morphology in these mice. We measured maximum bite force and jaw opening (i.e., gape) along with several musculoskeletal dimensions functionally linked to these performance measurements to test the hypotheses that GI mice evolved larger bite forces and jaw gapes as part of their extreme increase in size and/or novel diet. GI mice can bite more forcefully and open their jaws wider than a representative mainland strain of house mice. Similarly, GI mice have musculoskeletal features of the masticatory apparatus that are absolutely larger than WSB mice. However, when considered relative to body size or jaw length, as a relevant mechanical standard, GI mice show reduced performance, suggesting a size-related decrease in these abilities. Correspondingly, most musculoskeletal features are not relatively larger in GI mice. Incisor biting leverage and condylar dimensions are exceptions, suggesting relative increases in biting efficiency and condylar rotation in GI mice. Based on these results, we hypothesize that evolutionary enhancements in masticatory performance are correlated with the extreme increase in body size and associated musculoskeletal phenotypes in Gough Island mice. Anat Rec, 303:167-179, 2020. Extreme anatomies appear repeatedly throughout the evolutionary history of animals (e.g., Thomas and Reif, 1993). Island populations provide important contexts for studying divergence in animals (
Some of the most compelling examples of morphological evolution come from island populations. Alterations in the size and shape of the mandible have been repeatedly observed in murid rodents following island colonization. Despite this pattern and the significance of the mandible for dietary adaptation, the genetic basis of island-mainland divergence in mandibular form remains uninvestigated. To fill this gap, we examined mandibular morphology in 609 F2s from a cross between Gough Island mice, the largest wild house mice on record, and mice from a mainland reference strain (WSB). Univariate genetic mapping identifies three quantitative trait loci (QTL) for relative length of the temporalis lever arm and two distinct QTL for relative condyle length, two traits expected to affect mandibular function that differ between Gough Island mice and WSB mice. Multivariate genetic mapping of coordinates from geometric morphometric analyses identifies 27 QTL contributing to overall mandibular shape. QTL show a complex mixture of modest, additive effects dispersed throughout the mandible, with landmarks including the coronoid process and the base of the ascending ramus frequently modulated by QTL. Additive effects of most shape QTL do not align with island-mainland divergence, suggesting that directional selection played a limited role in the evolution of mandibular shape. In contrast, Gough Island mouse alleles at QTL for centroid size and QTL for jaw length increase these measures, suggesting selection led to larger mandibles, perhaps as a correlated response to the evolution of larger bodies.
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