Jean-Christophe Auffray

Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible?

Summary The mouse mandible has long served as a model system for studying the development and evolution of complex morphological structures. We used the methods of geometric morphometrics to reassess the hypothesis that the mandible consists of two separate modules: an anterior part bearing the teeth and a posterior part with muscle attachment surfaces and articulating with the skull. The analyses particularly focused on covariation of fluctuating asymmetry, because such covariation is due exclusively to direct interactions between the developmental processes that produce the traits of interest, whereas variation of traits among individuals also reflects other factors. The patterns of fluctuating asymmetry and individual variation were only partly consistent, indicating that developmental processes contribute differentially to variation at different levels. The results were in agreement with the hypothesis that the anterior and posterior parts of the mandible are separate develop‐mental modules. Comparison of all alternative partitions of the landmarks into two contiguous subsets confirmed the hypothesis for the location of the boundary between modules but also underscored that the separation between them is not complete. Modularity is therefore manifest as the relative independence of parts within the framework of overall integration of the mandible as a whole—it is a matter of degrees, not all or nothing.

Independence between developmental stability and canalization in the skull of the house mouse

The relationship between the two components of developmental homeostasis, that is canalization and developmental stability (DS), is currently debated. To appraise this relationship, the levels and morphological patterns of interindividual variation and fluctuating asymmetry were assessed using a geometric morphometric approach applied to the skulls of laboratory samples of the house mouse. These three samples correspond to two random–bred strains of the two European subspecies of the house mouse and their F1 hybrids. The inter– and intraindividual variation levels were found to be smaller in the hybrid group compared to the parental ones, suggesting a common heterotic effect on skull canalization and DS. Both buffering mechanisms might then depend on the same genetic condition, i.e. the level of heterozygosity. However, related morphological patterns did not exhibit any congruence. In contradiction with previous studies on insect wing traits, we therefore suggest that canalization and DS may not act on the same morphological characters. The fact that this discrepancy could be related to the functional importance of the symmetry of the characters under consideration is discussed in the light of our knowledge of the genetic bases of both components of developmental homeostasis.

Rapid chromosomal evolution in island mice

Madeira is a small volcanic island in the Atlantic Ocean with steep mountains separating narrow valleys that are the only areas habitable by humans and their commensals. Here we show that house mice (Mus musculus domesticus ) on Madeira have an unexpected chromosomal diversity, the evolution of which is independent of adaptive processes, relying instead on geographic isolation and genetic drift.

CONSERVED PHENOTYPIC VARIATION PATTERNS, EVOLUTION ALONG LINES OF LEAST RESISTANCE, AND DEPARTURE DUE TO SELECTION IN FOSSIL RODENTS

Abstract Within a group of organisms, some morphologies are more readily generated than others due to internal developmental constraints. Such constraints can channel evolutionary changes into directions corresponding to the greatest intraspecific variation. Long term evolutionary outputs, however, depend on the stability of these intraspecific patterns of variation over time and from the interplay between internal constraints and selective regimes. To address these questions, the relationship between the structure of phenotypic variance covariance matrices and direction of morphological evolution was investigated using teeth of fossil rodents. One lineage considered here leads to Stephanomys, a highly specialized genus characterized by a dental pattern supposedly favoring grass eating. Stephanomys evolved in the context of directional selection related to the climatic trend of global cooling causing an increasing proportion of grasslands in southwestern Europe. The initial divergence (up to 6.5 mya) was channeled along the direction of greatest intraspecific variation, whereas after 6.5 mya, morphological evolution departed from the direction favored by internal constraints. This departure from the “lines of least resistance” was likely the consequence of an environmental degradation causing a selective gradient strong enough to overwhelm the constraints to phenotypic evolution. However, in a context of stabilizing selection, these constraints actually channel evolution, as exemplified by the lineage of Apodemus. This lineage retained a primitive diet and dental pattern over the last 10 myr. Limited morphological changes occurred nevertheless in accordance with the main patterns of intraspecific variation. The importance of these lines of least resistance directing long‐term morphological evolution may explain parallel evolution of some dental patterns in murine evolution.

Environmental genetics: Rapid chromosomal evolution in islandmice

Madeira is a small volcanic island in the Atlantic Ocean with steep mountains separating narrow valleys that are the only areas habitable by humans and their commensals. Here we show that house mice (Mus musculus domesticus ) on Madeira have an unexpected chromosomal diversity, the evolution of which is independent of adaptive processes, relying instead on geographic isolation and genetic drift.

Ecological Correlates and Evolutionary Divergence in the Skull of Turtles: A Geometric Morphometric Assessment

Resource use and phylogeny are often correlated with morphological variation. Moreover, because biological shapes are often complex and evolve depending on several internal constraints, they must be assessed using integrative methods. We analyzed the morphological variation of the turtle skull in the context of an adaptive radiation. Our focus are turtles of the superfamily Testudinoidea, which are remarkably diverse, both in number of species and in ecology. In this study, we depict morphological variation in the turtle skull in three dimensions with respect to diet, phylogeny, and habitat using modern geometric morphometrics. Our study revealed that morphological specialization was related to both diet and habitat. Morphological variation is decomposed in regard of both resource use (habitat and diet) and phylogeny. Feeding mode depending on environment was suggested as a key factor determining morphological evolution and diversification of turtle skulls. Diet (especially durophagy) leads to parallel morphologies in different clades. Phylogeny seemed to constrain only localized features of the skull and remained of minor influence, because overall morphotypes, closely correlated with ecological factors, occurred in both clades. In conclusion, the adaptive radiation of the Testudinoidea is revealed to demonstrate a clear relationship between the skull shape and life style.

Genetic differentiation of the house mouse around the Mediterranean basin: matrilineal footprints of early and late colonization

The molecular signatures of the recent expansion of the western house mouse, Mus musculus domesticus, around the Mediterranean basin are investigated through the study of mitochondrial D-loop polymorphism on a 1313 individual dataset. When reducing the complexity of the matrilineal network to a series of haplogroups (HGs), our main results indicate that: (i) several HGs are recognized which seem to have almost simultaneously diverged from each other, confirming a recent expansion for the whole subspecies; (ii) some HGs are geographically delimited while others are widespread, indicative of multiple introductions or secondary exchanges; (iii) mice from the western and the eastern coasts of Africa harbour largely different sets of HGs; and (iv) HGs from the two shores of the Mediterranean are more similar in the west than in the east. This pattern is in keeping with the two-step westward expansion proposed by zooarchaeological data, an early one coincident with the Neolithic progression and limited to the eastern Mediterranean and a later one, particularly evident in the western Mediterranean, related to the generalization of maritime trade during the first millennium BC and onwards. The dispersal of mice along with humans, which continues until today, has for instance left complex footprints on the long ago colonized Cyprus or more simple ones on the much more recently populated Canary Islands.

Morphological evolution, ecological diversification and climate change in rodents

Among rodents, the lineage from Progonomys hispanicus to Stephanomys documents a case of increasing size and dental specialization during an approximately 9 Myr time-interval. On the contrary, some contemporaneous generalist lineages like Apodemus show a limited morphological evolution. Dental shape can be related to diet and can be used to assess the ecological changes along the lineages. Consequently, size and shape of the first upper molar were measured in order to quantify the patterns of morphological evolution along both lineages and compare them to environmental trends. Climatic changes do not have a direct influence on evolution, but they open new ecological opportunities by changing vegetation and allow the evolution of a specialist like Stephanomys. On the other hand, environmental changes are not dramatic enough to destroy the habitat of a long-term generalist like Apodemus. Hence, our results exemplify a case of an influence of climate on the evolution of specialist species, although a generalist species may persist without change.

DEVELOPMENTAL STABILITY, FITNESS, AND TRAIT SIZE IN LABORATORY HYBRIDS BETWEEN EUROPEAN SUBSPECIES OF THE HOUSE MOUSE

The effects of hybridization on developmental stability and size of tooth characters were investigated in intersubspecific crosses between random‐bred wild strains of the house mouse (Mus musculus domesticus and M. m. musculus). Fluctuating asymmetry (FA) and trait size were compared within and between parental, F1, backcross, and F2 hybrid groups. The relationship between FA and reproductive fitness within the F1 hybrids was also studied. The results indicated that both FA and character size levels differed significantly between the two subspecies. The F1 hybrids and the recombined groups (backcrosses and F2 hybrids) showed heterosis for both parameters. No significant differences in the FA of fertile and sterile F1 hybrid individuals were found. Comparison of the FA levels obtained in this study with those found in wild populations from the hybrid zone in Denmark showed that the levels of FA were lower in laboratory‐bred samples than in the wild populations. This study provides further evidence that, in hybrids, the developmental processes underlying most of the morphological traits we studied benefit from a heterotic effect, despite the genomic incompatibilities between the two European house mice revealed by previous genetical and parasitological studies.

Epigenetic effects on the mouse mandible: common features and discrepancies in remodeling due to muscular dystrophy and response to food consistency

BackgroundIn 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.ResultsFood 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.ConclusionsBone 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.