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Abstract Background Hybridization is often seen as a process dampening phenotypic differences accumulated between diverging evolutionary units. For a complex trait comprising several relatively independent modules, hybridization may however simply generate new phenotypes, by combining into a new mosaic modules inherited from each parental groups and parts intermediate with respect to the parental groups. We tested this hypothesis by studying mandible size and shape in a set of first and second generation hybrids resulting from inbred wild-derived laboratory strains documenting two subspecies of house mice, Musmusculus domesticus and Musmusculus musculus. Phenotypic variation of the mandible was divided into nested partitions of developmental, evolutionary and functional modules. Results The size and shape of the modules were differently influenced by hybridization. Some modules seemed to be the result of typical additive effects with hybrids intermediate between parents, some displayed a pattern expected in the case of monogenic dominance, whereas in other modules, hybrids were transgressive. The result is interpreted as the production of novel mandible morphologies. Beyond this modularity, modules in functional interaction tended to display significant covariations. Conclusions Modularity emerges as a source of novel morphological variation by its simple potential to combine different parts of the parental phenotypes into a novel offspring mosaic of modules. This effect is partly counterbalanced by bone remodeling insuring an integration of the mosaic mandible into a functional ensemble, adding a non-genetic component to the production of transgressive phenotypes in hybrids.

Abstract Background In wild populations phenotypic differentiation of skeletal structures is influenced by many factors including epigenetic interactions and plastic response to environmental influences, possibly blurring the expression of genetic differences. In contrast, laboratory animals provide the opportunity to separate environmental from genetic effects. The mouse mandible is particularly prone to such plastic variations because bone remodeling occurs late in postnatal ontogeny, in interaction with muscular loading. In order to understand the impact of this process on mandible morphology, we investigated how change in the masticatory function affects the mandible shape, and its pattern of variation. Breeding laboratory mice on food of different consistencies mimicked a natural variation in feeding ecology, whereas mice affected by the murine analogue of the Duchenne muscular dystrophy provided a case of pathological modification of the mastication process. Results Food consistency as well as dystrophy caused significant shape changes in the mouse mandible. Further differences were observed between laboratory strains and between sexes within strains, muscular dystrophy causing the largest morphological change. The directions of the morphological changes due to food consistency and muscular dystrophy were discrepant, despite the fact that both are related to bone remodeling. In contrast, directions of greatest variance were comparable among most groups, and the direction of the change due to sexual dimorphism was parallel to the direction of main variance. Conclusions Bone remodeling is confirmed as an important factor driving mandible shape differences, evidenced by differences due to both the consistency of the food ingested and muscular dystrophy. However, the resulting shape change will depend on how the masticatory function is affected. Muscular dystrophy caused shape changes distributed all over the mandible, all muscles being affected although possibly to a different degree. In contrast, the chewing function was mostly affected when the mice were fed on hard vs. soft food, whereas grinding likely occurred normally; accordingly, shape change was more localized. The direction of greatest variance, however, was remarkably comparable among groups, although we found a residual variance discarding age, sex, and food differences. This suggests that whatever the context in which bone remodeling occurs, some parts of the mandible such as the angular process are more prone to remodeling during late postnatal growth.

The semicircular canals of the inner ear are involved in balance and velocity control. Being crucial to ensure efficient mobility, their morphology exhibits an evolutionary conservatism attributed to stabilizing selection. Release of selection in slow‐moving animals has been argued to lead to morphological divergence and increased inter‐individual variation. In its natural habitat, the house mouse Mus musculus moves in a tridimensional space where efficient balance is required. In contrast, laboratory mice in standard cages are severely restricted in their ability to move, which possibly reduces selection on the inner ear morphology. This effect was tested by comparing four groups of mice: several populations of wild mice trapped in commensal habitats in France; their second‐generation laboratory offspring, to assess plastic effects related to breeding conditions; a standard laboratory strain (Swiss) that evolved for many generations in a regime of mobility reduction; and hybrids between wild offspring and Swiss mice. The morphology of the semicircular canals was quantified using a set of 3D landmarks and semi‐landmarks analyzed using geometric morphometric protocols. Levels of inter‐population, inter‐individual (disparity) and intra‐individual (asymmetry) variation were compared. All wild mice shared a similar inner ear morphology, in contrast to the important divergence of the Swiss strain. The release of selection in the laboratory strain obviously allowed for an important and rapid drift in the otherwise conserved structure. Shared traits between the inner ear of the lab strain and domestic pigs suggested a common response to mobility reduction in captivity. The lab‐bred offspring of wild mice also differed from their wild relatives, suggesting plastic response related to maternal locomotory behavior, since inner ear morphology matures before birth in mammals. The signature observed in lab‐bred wild mice and the lab strain was however not congruent, suggesting that plasticity did not participate to the divergence of the laboratory strain. However, contrary to the expectation, wild mice displayed slightly higher levels of inter‐individual variation than laboratory mice, possibly due to the higher levels of genetic variance within and among wild populations compared to the lab strain. Differences in fluctuating asymmetry levels were detected, with the laboratory strain occasionally displaying higher asymmetry scores than its wild relatives. This suggests that there may indeed be a release of selection and/or a decrease in developmental stability in the laboratory strain. [ABSTRACT FROM AUTHOR]

In molars without permanent eruption, wear deeply modifies the geometry of the crown. To test for a signature of diet on wear dynamics, the molar geometry was compared between commensal house mice, relying on an omnivorous-granivorous diet, and Sub-Antarctic relatives, characterized by a switch towards a more 'predatory' behaviour. Laboratory-bred offspring of commensal mice served as a reference by providing mice of known age. Molar geometry was quantified using dense 3D semi-landmark based descriptors of the whole molar row and the upper molar only. Laboratory offspring displayed a decreased rate of wear compared to their commensal relatives, due to reduced mastication in mice fed ad libitum. Sub-Antarctic mice displayed a similarly decreased rate of molar wear, in agreement with an optimization towards incisor biting to seize prey. Laboratory offspring and Sub-Antarctic mice were further characterized by straight molar rows, whereas in commensal mice, the erupting third molar deviated away from the longitudinal alignment with the other molars, due to masticatory loadings. Quantifying changes in molar geometry could thus contribute to trace subtle diet variations, and provide a direct insight into the constraints during mastication, shedding light on the functional role of adaptive changes in molar geometry. [ABSTRACT FROM AUTHOR]

Simple Summary: All life is derived from a single common ancestor, whose descendants coevolved with the planet, shaping the structure of biodiversity and the physical processes that operate on Earth. This complex history cannot be inferred solely by studying the genomes of living organisms, nor through analysis of the fossil remains of their extinct relatives. Only a unified approach integrating living and extinct species and drawing from both genomic and anatomical evidence can achieve this aim. In this review, we highlight recent advances, challenges, and opportunities in this endeavour. These include the development of models for analysis of anatomical data; methods for combined analysis of fossil and living species, as well as anatomical and genomic data; and the combined estimation of evolutionary relationships, geographic range, and evolutionary rates. However, the application of such methods is limited by a shortage of expertise in taxonomy and comparative anatomy, which are skills required for the compilation of anatomical datasets. Whereas there is a common concern for the incompleteness of the fossil record, knowledge with respect to the comparative anatomy of living species is equally incomplete. We anticipate that the increased demand for an integrative phylogenetic approach to reconstruct the tree of life and evolutionary patterns and processes will encourage researchers to overcome these challenges with the aim of elucidating the complexities behind organismal evolution across broad taxonomic and time scales. The modern era of analytical and quantitative palaeobiology has only just begun, integrating methods such as morphological and molecular phylogenetics and divergence time estimation, as well as phenotypic and molecular rates of evolution. Calibrating the tree of life to geological time is at the nexus of many disparate disciplines, from palaeontology to molecular systematics and from geochronology to comparative genomics. Creating an evolutionary time scale of the major events that shaped biodiversity is key to all of these fields and draws from each of them. Different methodological approaches and data employed in various disciplines have traditionally made collaborative research efforts difficult among these disciplines. However, the development of new methods is bridging the historical gap between fields, providing a holistic perspective on organismal evolutionary history, integrating all of the available evidence from living and fossil species. Because phylogenies with only extant taxa do not contain enough information to either calibrate the tree of life or fully infer macroevolutionary dynamics, phylogenies should preferably include both extant and extinct taxa, which can only be achieved through the inclusion of phenotypic data. This integrative phylogenetic approach provides ample and novel opportunities for evolutionary biologists to benefit from palaeontological data to help establish an evolutionary time scale and to test core macroevolutionary hypotheses about the drivers of biological diversification across various dimensions of organisms. [ABSTRACT FROM AUTHOR]