ABSTRACT
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.
Subject(s)
Biological Evolution , Semicircular Canals , Animals , Mice , Semicircular Canals/anatomy & histology , Mammals , FranceABSTRACT
Small mammal species play an important role influencing vegetation primary productivity and plant species composition, seed dispersal, soil structure, and as predator and/or prey species. Species which experience population dynamics cycles can, at high population phases, heavily impact agricultural sectors and promote rodent-borne disease transmission. To better understand the drivers behind small mammal distributions and abundances, and how these differ for individual species, it is necessary to characterise landscape variables important for the life cycles of the species in question. In this study, a suite of Earth observation derived metrics quantifying landscape characteristics and dynamics, and in-situ small mammal trapline and transect survey data, are used to generate random forest species distribution models for nine small mammal species for study sites in Narati, China and Sary Mogul, Kyrgyzstan. These species distribution models identify the important landscape proxy variables driving species abundance and distributions, in turn identifying the optimal conditions for each species. The observed relationships differed between species, with the number of landscape proxy variables identified as important for each species ranging from 3 for Microtus gregalis at Sary Mogul, to 26 for Ellobius tancrei at Narati. Results indicate that grasslands were predicted to hold higher abundances of Microtus obscurus, E. tancrei and Marmota baibacina, forest areas hold higher abundances of Myodes centralis and Sorex asper, with mixed forest-grassland boundary areas and areas close to watercourses predicted to hold higher abundances of Apodemus uralensis and Sicista tianshanica. Localised variability in vegetation and wetness conditions, as well as presence of certain habitat types, are also shown to influence these small mammal species abundances. Predictive application of the Random Forest (RF) models identified spatial hot-spots of high abundance, with model validation producing R2 values between 0.670 for M. gregalis transect data at Sary Mogul to 0.939 for E. tancrei transect data at Narati. This enhances previous work whereby optimal habitat was defined simply as presence of a given land cover type, and instead defines optimal habitat via a combination of important landscape dynamic variables, moving from a human-defined to species-defined perspective of optimal habitat. The species distribution models demonstrate differing distributions and abundances of host species across the study areas, utilising the strengths of Earth observation data to improve our understanding of landscape and ecological linkages to small mammal distributions and abundances.
Subject(s)
Advance Directives , Mammals , Humans , Animals , Agriculture , Arvicolinae , Benchmarking , Marmota , MurinaeABSTRACT
Rodent outbreaks have plagued European agriculture for centuries, but continue to elude comprehensive explanation. Modelling and empirical work in some cyclic rodent systems suggests that changes in reproductive parameters are partly responsible for observed population dynamics. Using a 17-year time series of Microtus arvalis population abundance and demographic data, we explored the relationship between meteorological conditions (temperature and rainfall), female reproductive activity, and population growth rates in a non-cyclic population of this grassland vole species. We found strong but complex relationships between female reproduction and climate variables, with spring female reproduction depressed after cold winters. Population growth rates were, however, uncorrelated with either weather conditions (current and up to three months prior) or with female reproduction (number of foetuses per female and/or proportion of females reproductively active in the population). These results, coupled with age-structure data, suggest that mortality, via predation, disease, or a combination of the two, are responsible for the large multi-annual but non-cyclic population dynamics observed in this population of the common vole.
Subject(s)
Arvicolinae/physiology , Biomass , Fertility , Litter Size , Weather , Animals , Ecosystem , Female , Male , Periodicity , ReproductionABSTRACT
Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior-lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.
Subject(s)
Arvicolinae/genetics , Evolution, Molecular , Genetic Variation , Genetics, Population , Adaptation, Biological/genetics , Animals , Arvicolinae/anatomy & histology , Climate , Ecosystem , Europe , Founder Effect , Islands , Models, Genetic , Molar/anatomy & histology , Phenotype , ScotlandABSTRACT
Oceanic islands have been a test ground for evolutionary theory, but here, we focus on the possibilities for evolutionary study created by offshore islands. These can be colonized through various means and by a wide range of species, including those with low dispersal capabilities. We use morphology, modern and ancient sequences of cytochrome b (cytb) and microsatellite genotypes to examine colonization history and evolutionary change associated with occupation of the Orkney archipelago by the common vole (Microtus arvalis), a species found in continental Europe but not in Britain. Among possible colonization scenarios, our results are most consistent with human introduction at least 5100 bp (confirmed by radiocarbon dating). We used approximate Bayesian computation of population history to infer the coast of Belgium as the possible source and estimated the evolutionary timescale using a Bayesian coalescent approach. We showed substantial morphological divergence of the island populations, including a size increase presumably driven by selection and reduced microsatellite variation likely reflecting founder events and genetic drift. More surprisingly, our results suggest that a recent and widespread cytb replacement event in the continental source area purged cytb variation there, whereas the ancestral diversity is largely retained in the colonized islands as a genetic 'ark'. The replacement event in the continental M. arvalis was probably triggered by anthropogenic causes (land-use change). Our studies illustrate that small offshore islands can act as field laboratories for studying various evolutionary processes over relatively short timescales, informing about the mainland source area as well as the island.
Subject(s)
Arvicolinae/genetics , Biological Evolution , Genetics, Population , Islands , Animal Distribution , Animals , Arvicolinae/anatomy & histology , Bayes Theorem , Belgium , Cytochromes b/genetics , DNA, Mitochondrial/genetics , Microsatellite Repeats , Molecular Sequence Data , Phylogeny , United KingdomABSTRACT
From continental to regional scales, the zoonosis alveolar echinococcosis (AE) (caused by Echinococcus multilocularis) forms discrete patches of endemicity within which transmission hotspots of much larger prevalence may occur. Since the late 80s, a number of hotspots have been identified in continental Asia, mostly in China, wherein the ecology of intermediate host communities has been described. This is the case in south Gansu, at the eastern border of the Tibetan plateau, in south Ningxia, in the western Tian Shan of Xinjiang, and in the Alay valley of south Kyrgyzstan. Here we present a comparative natural history and characteristics of transmission ecosystems or ecoscapes. On this basis, regional types of transmission and their ecological characteristics have been proposed in a general framework. Combining climatic, land cover and intermediate host species distribution data, we identified and mapped 4 spatially distinct types of transmission ecosystems typified by the presence of one of the following small mammal 'flagship' species: Ellobius tancrei, Ochotona curzoniae, Lasiopodomys brandtii or Eospalax fontanierii. Each transmission ecosystem had its own characteristics which can serve as a reference for further in-depth research in the transmission ecology of E. multilocularis. This approach may be used at fine spatial scales to characterize other poorly known transmission systems of the large Eurasian endemic zone, and help in consideration of surveillance systems and interventions.
Subject(s)
Arvicolinae/parasitology , DNA, Helminth/genetics , Echinococcosis, Hepatic/transmission , Echinococcosis, Hepatic/veterinary , Echinococcus multilocularis/isolation & purification , Lagomorpha/parasitology , Wolves/parasitology , Animal Distribution , Animals , Asia, Central/epidemiology , China/epidemiology , Disease Vectors , Echinococcosis , Echinococcosis, Hepatic/epidemiology , Echinococcosis, Hepatic/parasitology , Echinococcus multilocularis/genetics , Ecosystem , Feces/parasitology , Host Specificity , Humans , Phylogeography , Species SpecificityABSTRACT
Phenotype variation is a key feature in evolution, being produced by development and the target of the screening by selection. We focus here on a variable morphological feature: the third upper molar (UM3) of the bank vole, aiming at identifying the sources of this variation. Size and shape of the UM3 occlusal surface was quantified in successive samples of a bank vole population. The first source of variation was the season of trapping, due to differences in the age structure of the population in turn affecting the wear of the teeth. The second direction of variation corresponded to the occurrence, or not, of an additional triangle on the tooth. This intra-specific variation was attributed to the space available at the posterior end of the UM3, allowing or not the addition of a further triangle.This size variation triggering the shape polymorphism is not controlled by the developmental cascade along the molar row. This suggests that other sources of size variation, possibly epigenetic, might be involved. They would trigger an important shape variation as side-effect by affecting the termination of the sequential addition of triangles on the tooth.
Subject(s)
Arvicolinae/anatomy & histology , Models, Anatomic , Tooth/anatomy & histology , Animals , Arvicolinae/growth & development , Biological Evolution , Molar/anatomy & histology , Molar/growth & development , Tooth/growth & developmentABSTRACT
Morphological integration corresponds to interdependency between characters that can arise from several causes. Proximal causes of integration include that different phenotypic features may share common genetic sets and/or interact during their development. Ultimate causes may be the prolonged effect of selection favoring integration of functionally interacting characters, achieved by the molding of these proximal causes. Strong and direct interactions among successive teeth of a molar row are predicted by genetic and developmental evidences. Functional constraints related to occlusion, however, should have selected more strongly for a morphological integration of occluding teeth and a corresponding evolution of the underlying developmental and genetic pathways. To investigate how these predictions match the patterns of phenotypic integration, we studied the co-variation among the six molars of the murine molar row, focusing on two populations of house mice (Mus musculus domesticus) and wood mice (Apodemus sylvaticus). The size and shape of the three upper and lower molars were quantified and compared. Our results evidenced similar patterns in both species, size being more integrated than shape among all the teeth, and both size and shape co-varying strongly between adjacent teeth, but also between occluding teeth. Strong co-variation within each molar row is in agreement with developmental models showing a cascade influence of the first molar on the subsequent molars. In contrast, the strong co-variation between molars of the occluding tooth rows confirms that functional constraints molded patterns of integration and probably the underlying developmental pathways despite the low level of direct developmental interactions occurring among molar rows. These patterns of co-variation are furthermore conserved between the house mouse and the wood mouse that diverged >10 Ma, suggesting that they may constitute long-running constraints to the diversification of the murine rodent dentition.
Subject(s)
Biological Evolution , Genetic Variation , Germ Cells/cytology , Mice/embryology , Animals , Selection, GeneticABSTRACT
The Pyrenean region exhibits high levels of endemism suggesting a major contribution to the phylogeography of European species. But, to date, the role of the Pyrenees and surrounding areas as a glacial refugium for temperate species remains poorly explored. In the current study, we investigated the biogeographic role of the Pyrenean region through the analyses of genetic polymorphism and morphology of a typical forest-dwelling small mammal, the bank vole (Myodes glareolus). Analyses of the mitochondrial cytochrome b gene and the third upper molar (M(3)) show a complex phylogeographic structure in the Pyrenean region with at least three distinct lineages: the Western European, Spanish and Basque lineages. The Basque lineage in the northwestern (NW) Pyrenees was identified as a new clearly differentiated and geographically localized bank vole lineage in Europe. The average M(3) shape of Basque bank voles suggests morphological differentiation but also restricted genetic exchanges with other populations. Our genetic and morphological results as well as palaeo-environmental and fossils records support the hypothesis of a new glacial refugium in Europe situated in the NW Pyrenees. The permissive microclimatic conditions that prevailed for a long time in this region may have allowed the survival of temperate species, including humans. Moreover, local differentiation around the Pyrenees is favoured by the opportunity for populations to track the shift of the vegetation belt in altitude rather than in latitude. The finding of the Basque lineage is in agreement with the high level of endemic taxa reported in the NW Pyrenees.
Subject(s)
Arvicolinae/genetics , Genetics, Population , Phylogeny , Animals , Arvicolinae/anatomy & histology , Cytochromes b/genetics , DNA, Mitochondrial/genetics , Europe , Evolution, Molecular , Geography , Haplotypes , Polymorphism, Genetic , Sequence Analysis, DNAABSTRACT
We investigate the relationship between landscape heterogeneity and the spatial distribution of small mammals in two areas of Western Sichuan, China. Given a large diversity of species trapped within a large number of habitats, we first classified small mammal assemblages and then modelled the habitat of each in the space of quantitative environmental descriptors. Our original two step "classify then model" procedure is appropriate for the frequently encountered study scenario: trapping data collected in remote areas with sampling guided by expert field knowledge.In the classification step, we defined assemblages by grouping sites of similar species composition and relative densities using an expert-class-merging procedure which reduced redundancy in the habitat factor used within a multinomial logistic regression predicting species trapping probabilities. Assemblages were thus defined as mixtures of small mammal frequency distributions in discrete groups of sampled sites.In the modelling step, assemblages' habitats and environments of the two sampled areas were discriminated in the space of remotely sensed environmental descriptors. First, we compared the discrimination of assemblage/study areas by linear and non-linear forms of Discriminant Analysis (Linear Discriminant Analysis versus Mixture Discriminant Analysis) and of Multiple Regression (Generalized Linear Models versus Multiple Adaptive Regression Splines). The "best" predictive modelling technique was then used to quantify the contribution of each environmental variable in discriminations of assemblages and areas.Mixtures of Gaussians provided a more efficient model of assemblage coverage in environmental space than a single Gaussian cluster model. However, non-linearity in assemblage response to environmental gradients was consistently predicted with lower deviance and misclassification error by Multiple Adaptive Regression Splines. The two study areas were mainly discriminated along vegetation indices. However, although the Normalized Difference Vegetation Index (NDVI) could discriminate forested from non-forested habitats, its power to discriminate assemblages in Maerkang, where a greater diversity of forest habitat was observed, was seen to be limited, and in this case NDVI was outperformed by the Enhanced Vegetation Index (EVI). Our analyses highlight previously unobserved differences between the environments and small mammal communities of two fringe areas of the Tibetan plateau and suggests that a biogeograph-ical approach is required to elucidate ecological processes in small mammal communities and to reduce extrapolation uncertainty in distribution mapping.
ABSTRACT
Elucidating the colonization processes associated with Quaternary climatic cycles is important in order to understand the distribution of biodiversity and the evolutionary potential of temperate plant and animal species. In Europe, general evolutionary scenarios have been defined from genetic evidence. Recently, these scenarios have been challenged with genetic as well as fossil data. The origins of the modern distributions of most temperate plant and animal species could predate the Last Glacial Maximum. The glacial survival of such populations may have occurred in either southern (Mediterranean regions) and/or northern (Carpathians) refugia. Here, a phylogeographic analysis of a widespread European small mammal (Microtus arvalis) is conducted with a multidisciplinary approach. Genetic, fossil and ecological traits are used to assess the evolutionary history of this vole. Regardless of whether the European distribution of the five previously identified evolutionary lineages is corroborated, this combined analysis brings to light several colonization processes of M. arvalis. The species' dispersal was relatively gradual with glacial survival in small favourable habitats in Western Europe (from Germany to Spain) while in the rest of Europe, because of periglacial conditions, dispersal was less regular with bottleneck events followed by postglacial expansions. Our study demonstrates that the evolutionary history of European temperate small mammals is indeed much more complex than previously suggested. Species can experience heterogeneous evolutionary histories over their geographic range. Multidisciplinary approaches should therefore be preferentially chosen in prospective studies, the better to understand the impact of climatic change on past and present biodiversity.
Subject(s)
Animal Migration/physiology , Arvicolinae/genetics , Arvicolinae/physiology , Fossils , Animals , Cytochromes b/genetics , Demography , Europe , Gene Flow/physiology , Genetic Speciation , Genetic Variation/physiology , Phylogeny , Sequence Analysis, DNAABSTRACT
A striking feature of the transmission ecology of Echinococcus multilocularis in China is the diversity of hosts that contribute to the parasite cycle. Considering the population dynamics of key reservoir intermediate hosts and the ratio of their preferred habitat in a landscape (ROMPA) is essential to understanding transmission, but the numerous communities in which the parasite cycles and the extent of those communities is currently far from being fully documented. On the Tibetan plateau grassland management influences intermediate host species populations and the sheer size of the area could be a major contributing factor to sustaining transmission in the region. In Southern Gansu and Southern Ningxia the processes of deforestation have temporarily provided optimal habitat for key reservoir intermediate hosts of E. multilocularis, resulting in high transmission and human disease, however currently the parasite may be extinct locally. Faced with this pattern of potentially transient transmission in a diversity of communities the question of the dispersal potential of the parasite arises. The reforestation program currently active across much of Western China has the potential to give rise to a massive increase in habitat favourable to suitable intermediate hosts and emergence or re-emergence of the zoonosis alveolar echinococcosis in many areas. This potential epidemic could be mitigated by both natural and human induced parasite dispersal mechanisms including fox migration and the sale of infected dogs originating from stable endemic foci on the Tibetan plateau. However, currently the degree of genetic exchange between discrete transmission foci is unknown and it is expected that genetic techniques could provide crucial information regarding this important question.
Subject(s)
Echinococcosis/transmission , Echinococcus multilocularis/physiology , Lagomorpha/parasitology , Rodentia/parasitology , Animals , China/epidemiology , Echinococcosis/epidemiology , Echinococcosis/parasitology , Ecology , Host-Parasite Interactions , HumansABSTRACT
Populations of common voles Microtus arvalis were studied as hosts of the tapeworm Taenia taeniaeformis during a 14-yr survey. They were monitored in spring, summer, and autumn in a pastoral ecosystem in eastern France. A total of 7,574 voles were sampled during 2 multiannual population fluctuations. A third fluctuation was sampled during the increase phase only. Overall prevalence was lowest in summer (0.6%), increased by 3 times in autumn (1.5%) and a further 5 times in spring (7.8%). Analysis of prevalence, based on 7,384 voles, by multiple logistic regression revealed that extrinsic factors such as season and intrinsic factors such as host age and host density have a combined effect. In the longer term, host age and host density were positively associated with prevalence in summer. Host density was strongly associated with autumn prevalence. There was no association between the fluctuation phase and prevalence. The study shows that a long timescale (here a multiannual survey) is necessary to demonstrate the positive effect of host density on the prevalence of this indirectly transmitted parasite. The demonstration of this relationship depends on the rodents being intermediate rather than definitive hosts.