Sex-specific selection on energy metabolism - selection coefficients for winter survival

Selection for different fitness optima between sexes is supposed to operate on several traits. As fitness-related traits are often energetically costly, selection should also act directly on the energetics of individuals. However, efforts to examine the relationship between fitness and components of the energy budget are surprisingly scarce. We investigated the effects of basal metabolic rate (BMR, the minimum energy required for basic life functions) and body condition on long-term survival (8 winter months) with manipulated densities in enclosed populations of bank voles (Myodes glareolus). Here, we show that survival selection on BMR was clearly sex-specific but density-independent. Both…

The effect of chronic low-dose environmental radiation on organ mass of bank voles in the Chernobyl Exclusion Zone

Purpose: Animals are exposed to environmental ionizing radiation (IR) externally through proximity to contaminated soil and internally through ingestion and inhalation of radionuclides. Internal organs can respond to radioactive contamination through physiological stress. Chronic stress can compromise the size of physiologically active organs, but studies on wild mammal populations are scarce. The effects of environmental IR contamination on organ masses was studied by using a wild rodent inhabiting the Chernobyl Exclusion Zone (CEZ). Material and Methods: The masses of brain, heart, kidney, spleen, liver and lung were assessed from bank voles (Myodes glareolus) captured from areas across r…

Molecular and ecological signs of mitochondrial adaptation: consequences for introgression?

The evolution of the mitochondrial genome and its potential adaptive impact still generates vital debates. Even if mitochondria have a crucial functional role, as they are the main cellular energy suppliers, mitochondrial DNA (mtDNA) introgression is common in nature, introducing variation in populations upon which selection may act. Here we evaluated whether the evolution of mtDNA in a rodent species affected by mtDNA introgression is explained by neutral expectations alone. Variation in one mitochondrial and six nuclear markers in Myodes glareolus voles was examined, including populations that show mtDNA introgression from its close relative, Myodes rutilus. In addition, we modelled prote…

Unravelling biodiversity, evolution and threats to conservation in the Sahara-Sahel

Deserts and arid regions are generally perceived as bare and rather homogeneous areas of low diversity. The Sahara is the largest warm desert in the world and together with the arid Sahel displays high topographical and climatic heterogeneity, and has experienced recent and strong climatic oscillations that have greatly shifted biodiversity distribution and community composition. The large size, remoteness and long-term political instability of the Sahara-Sahel, have limited knowledge on its biodiversity. However, over the last decade, there have been an increasing number of published scientific studies based on modern geomatic and molecular tools, and broad sampling of taxa of these region…

Maintenance costs of male dominance and sexually antagonistic selection in the wild

Variation in dominance status determines male mating and reproductive success, but natural selection for male dominance can be detrimental or antagonistic for female performance, and ultimately their fitness. Attaining and maintaining a high dominance status in a population of competing individuals is physiologically costly for males. But how male dominance status is mediated by maintenance energetics is currently not well understood, nor are the corresponding effects of male energetics on his sisters recognized. We conducted laboratory and field experiments on rodent populations to test whether selective breeding for male dominance status (dominant vs. subordinate breeding lines) antagonis…

Do colour morphs of wall lizards express different personalities?

Abstract Colour morphs sometimes have different behavioural strategies which may be maintained by frequency or density dependence mechanisms. We investigated temporal changes in behavioural reaction to a novel environment among colour morphs (yellow, orange, white) of the European wall lizard (Podarcis muralis). Adult males were given two 15 min experimental trials, and their locomotion was highly consistent between the two trials. Boldness, freezing and escape behaviour were less repeatable. Colour morphs differed in their locomotion and freezing behaviour. Boldness was similar among the morphs, whereas escape behaviour was lowest in yellow morph. Consequently, yellow morph males tended to…

Comparable response of wild rodent gut microbiome to anthropogenic habitat contamination

Abstract Species identity is thought to dominate over environment in shaping wild rodent gut microbiota, but it remains unknown whether the responses of host gut microbiota to shared anthropogenic habitat impacts are species-specific or if the general gut microbiota response is similar across host species. Here, we compare the influence of exposure to radionuclide contamination on the gut microbiota of four wild mouse species: Apodemus flavicollis, A. sylvaticus, A. speciosus and A. argenteus. Building on the evidence that radiation impacts bank vole (Myodes glareolus) gut microbiota, we hypothesized that radiation exposure has a general impact on rodent gut microbiota. Because we sampled (…

Camouflage in arid environments: the case of Sahara-Sahel desert rodents

Deserts and semi-deserts, such as the Sahara-Sahel region in North Africa, are exposed environments with restricted vegetation coverage. Due to limited physical surface structures, these open areas provide a promising ecosystem to understand selection for crypsis. Here, we review knowledge on camouflage adaptation in the Sahara-Sahel rodent community, which represents one of the best documented cases of phenotype-environment convergence comprising a marked taxonomic diversity. Through their evolutionary history, several rodent species from the Sahara-Sahel have repeatedly evolved an accurate background matching against visually-guided predators. Top-down selection by predators is therefore …

Introgression of mitochondrial DNA among Myodes voles: consequences for energetics?

Abstract Background Introgression of mitochondrial DNA (mtDNA) is among the most frequently described cases of reticulate evolution. The tendency of mtDNA to cross interspecific barriers is somewhat counter-intuitive considering the key function of enzymes that it encodes in the oxidative-phosphorylation process, which could give rise to hybrid dysfunction. How mtDNA reticulation affects the evolution of metabolic functions is, however, uncertain. Here we investigated how morpho-physiological traits vary in natural populations of a common rodent (the bank vole, Myodes glareolus) and whether this variation could be associated with mtDNA introgression. First, we confirmed that M. glareolus ha…

The origin of two cryptic species of African desert jerboas (Dipodidae: Jaculus)

The desert biota is exposed to extreme and variable conditions that shape its evolution and diversification processes. In this respect, the Jaculus jerboas have gained the attention of researchers as a result of their broad Saharan–Arabian distribution and their high and unexplained, morphological, anatomical, and molecular variation. In the present study, mitochondrial and nuclear genealogies where used to confirm monophyly of two cryptic species: Jaculus jaculus and Jaculus deserti. The reconstructed demography showed that the evolutionary histories of the species are markedly different and that the expansion into North-West Africa by J. deserti was more recent than that of J. jaculus. Th…

Exposure to environmental radionuclides associates with tissue-specific impacts on telomerase expression and telomere length

International audience; Telomeres, the protective structures at the ends of chromosomes, can be shortened when individuals are exposed to stress. In some species, the enzyme telomerase is expressed in adult somatic tissues, and potentially protects or lengthens telomeres. Telomeres can be damaged by ionizing radiation and oxidative stress, although the effect of chronic exposure to elevated levels of radiation on telomere maintenance is unknown for natural populations. We quantified telomerase expression and telomere length (TL) in different tissues of the bank vole Myodes glareolus, collected from the Chernobyl Exclusion Zone, an environment heterogeneously contaminated with radionuclides,…

The effect of spatial and temporal scale on camouflage in North African rodents

Abstract Background matching, a common form of camouflage, is a widespread anti-predator adaptation that hinders detection or recognition by increasing the resemblance of prey to its environment. However, the natural environment is complex and both spatially and temporally variable, which constrains effective background matching as an anti-predator strategy. Here, using remote sensing data (publicly available satellite imagery), we investigated how variation of habitat parameters predicts background matching in 16 Sahara–Sahel rodent species across spatial and temporal scales. All fur colour parameters (hue, saturation and brightness) strongly matched the respective habitats of the differen…

Chronic Background Radiation Correlates With Sperm Swimming Endurance in Bank Voles From Chernobyl

Sperm quantity and quality are key features explaining intra- and interspecific variation in male reproductive success. Spermatogenesis is sensitive to ionizing radiation and laboratory studies investigating acute effects of ionizing radiation have indeed found negative effects of radiation on sperm quantity and quality. In nature, levels of natural background radiation vary dramatically, and chronic effects of low-level background radiation exposure on spermatogenesis are poorly understood. The Chernobyl region offers a unique research opportunity for investigating effects of chronic low-level ionizing radiation on reproductive properties of wild organisms. We captured male bank voles (Myo…

The association between body mass, metabolic rates and survival of bank voles

Summary 1Many studies have been performed in an attempt to explain physiological, ecological and evolutionary factors behind inter- and intraspecific variation in basal metabolic rate (BMR) and maximum aerobic metabolic rate (VO2max). However, very little is known about the association between the traits and fitness components in populations of free-living animals. 2We studied the association between body size and the metabolic rates of bank voles Myodes (= Clethrionomys) glareolus and their survival, measured by repeated trappings across 2 years in an isolated, island population. All measured traits (body mass, BM; head width, HW; VO2max and BMR) were significantly repeatable over short (m…

Additional file 1 of Evolutionary history of two cryptic species of northern African jerboas

Additional file 1: Microsatellite optimization. Supplementary Tables and Figures.

Applying the Anna Karenina principle for wild animal gut microbiota : temporal stability of the bank vole gut microbiota in a disturbed environment

Gut microbiota play an important role in host health. Yet, the drivers and patterns of microbiota imbalance (dysbiosis) in wild animals remain largely unexplored. One hypothesised outcome of stress on animal microbiomes is a destabilised microbial community that is characterised by an increase in inter-individual differences compared with microbiomes of healthy animals, which are expected to be (i) temporally stable and (ii) relatively similar among individuals. This set of predictions for response of microbiomes to stressors is known as the Anna Karenina principle (AKP) for animal microbiomes. We examine the AKP in a wild mammal inhabiting disturbed environments by conducting a capture-mar…

Chronic Background Radiation Correlates With Sperm Swimming Endurance in Bank Voles From Chernobyl

Sperm quantity and quality are key features explaining intra- and interspecific variation in male reproductive success. Spermatogenesis is sensitive to ionizing radiation and laboratory studies investigating acute effects of ionizing radiation have indeed found negative effects of radiation on sperm quantity and quality. In nature, levels of natural background radiation vary dramatically, and chronic effects of low-level background radiation exposure on spermatogenesis are poorly understood. The Chernobyl region offers a unique research opportunity for investigating effects of chronic low-level ionizing radiation on reproductive properties of wild organisms. We captured male bank voles (Myo…

Interpretation of gut microbiota data in the ‘eye of the beholder’: A commentary and re‐evaluation of data from ‘Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone’

1.Evidence that exposure to environmental pollutants can alter the gut microbiota composition of wildlife includes studies of rodents exposed to radionuclides. 2.Antwis et al. (2021) used amplicon sequencing to characterise the gut microbiota of four species of rodent (Myodes glareolus, Apodemus agrarius, A. flavicollis and A. sylvaticus) inhabiting the Chernobyl Exclusion Zone (CEZ) to examine possible changes in gut bacteria (microbiota) and gut fungi (mycobiota) associated with exposure to radionuclides and whether the sample type (from caecum or faeces) affected the analysis. 3.The conclusions derived from the analyses of gut mycobiota are based on data that represent a mixture of inges…

Sexual and natural selection on body mass and metabolic rates in free-living bank voles

Summary 1. Because energy is a crucial resource, adaptive significance of variation in the rate of energy metabolism, and especially in basal (BMR) and maximum aerobic (VO2max) metabolic rates, is a popular theme in evolutionary and ecological physiology. However, little is known about the association of these traits with fitness components in populations of free-living animals. 2. We studied the association between body size, the metabolic rates, and reproductive success in bank voles (Myodes glareolus) in an isolated, small island population. Correlation analyses were performed for two measures of reproductive performance: mating success (the number of partners with which an individual ha…

Ecological mechanisms can modify radiation effects in a key forest mammal of Chernobyl

International audience; Nuclear accidents underpin the need to quantify the ecological mechanisms which determine injury to ecosystems from chronic low-dose radiation. Here, we tested the hypothesis that ecological mechanisms interact with ionizing radiation to affect natural populations in unexpected ways. We used large-scale replicated experiments and food manipulations in wild populations of the rodent, Myodes glareolus, inhabiting the region near the site of the Chernobyl disaster of 1986. We show linear decreases in breeding success with increasing ambient radiation levels with no evidence of any threshold below which effects are not seen. Food supplementation of experimental populatio…

Phylogeography of two cryptic species of African desert jerboas (Dipodidae: Jaculus)

The lesser Egyptian jerboa Jaculus jaculus is a desert dwelling rodent that inhabits a broad Arabian–Saharan arid zone. Recently, two distant sympatric lineages were described in North-West Africa, based on morphometric and molecular data, which may correspond to two cryptic species. In the current study, phylogenetic relationships and phylogeographical structure among those lineages and geographical populations from North Africa and the Middle East were investigated. The phylogeographical patterns and genetic diversity of the cytochrome b gene (1110 bp) were addressed on 111 jerboas from 41 localities. We found that the variation in Africa is partitioned into two divergent mitochondrial cl…

Applying the Anna Karenina principle for wild animal gut microbiota: Temporal stability of the bank vole gut microbiota in a disturbed environment.

Gut microbiota play an important role in host health. Yet, the drivers and patterns of microbiota imbalance (dysbiosis) in wild animals remain largely unexplored. One hypothesised outcome of stress on animal microbiomes is a destabilised microbial community that is characterised by an increase in inter-individual differences compared with microbiomes of healthy animals, which are expected to be (a) temporally stable and (b) relatively similar among individuals. This set of predictions for response of microbiomes to stressors is known as the Anna Karenina principle (AKP) for animal microbiomes. We examine the AKP in a wild mammal inhabiting disturbed environments by conducting a capture-mark…

Camouflage accuracy in Sahara-Sahel desert rodents

1.Camouflage helps animals to hide from predators and is therefore key to survival. Although widespread convergence of animal phenotypes to their natural environment is well established, there is a lack of knowledge about how species compromise camouflage accuracy across different background types in their habitat. 2.Here we tested how background matching has responded to top‐down selection by avian and mammalian predators using Sahara‐Sahel desert rodents in North Africa. 3.We show that the fur coloration of several species has become an accurate match to different types of desert habitats. This is supported by a correlation analysis of colour and pattern metrics, investigation of animal‐t…

On personality, energy metabolism and mtDNA introgression in bank voles

Consistent interindividual differences in behaviour, or animal personality, are emerging as an important determinant of a wide range of life history traits and fitness. Individual behaviour, however, may be constrained by between-individual variability in energy metabolism and may become unstable owing to intrinsic and extrinsic stressors. Here we tested the relationship between personality and physiology using wild-caught bank voles, Myodes glareolus, that varied according to mtDNA type (original or introgressed from Myodes rutilus). Personality traits and their within-individual consistency were assessed using an open field test and basal metabolic rate (BMR) was measured in an open-flow …

Camouflage accuracy in Sahara–Sahel desert rodents

1. Camouflage helps animals to hide from predators and is therefore key to survival. Although widespread convergence of animal phenotypes to their natural environment is well-established, there is a lack of knowledge about how species compromise camouflage accuracy across different background types in their habitat.2. Here we tested how background matching has responded to top–down selection by avian and mammalian predators using Sahara–Sahel desert rodents in North Africa.3. We show that the fur colouration of several species has become an accurate match to different types of desert habitats. This is supported by a correlation analysis of colour and pattern metrics, investigation of animal…

Large Spatial Scale of the Phenotype-Environment Color Matching in Two Cryptic Species of African Desert Jerboas (Dipodidae: Jaculus)

We tested the camouflage hypothesis, or the linkage between animal (Saharan rodent) and habitat coloration, on the largest geographical scale yet conducted. We aimed to determine whether phenotypic variation is explained by micro-habitat variation and/or genetic polymorphism to determine 1) the strength of linkage between fur color and local substrate color, and 2) the divergence in fur coloration between two genetic clades, representing cryptic species, throughout the complete range of the African desert jerboas (Jaculus jaculus). We used a combination of museum and field-collected specimens, remote sensing tools, satellite and digital photography and molecular genetic and phylogenetic met…

Analysis of heteroplasmy in bank voles inhabiting the Chernobyl exclusion zone : A commentary on Baker et al. (2017) "Elevated mitochondrial genome variation after 50 generations of radiation exposure in a wild rodent."

Evolutionary history of two cryptic species of northern African jerboas

Abstract Background: Climatic variation and geologic change both play significant roles in shaping species distributions, thus affecting their evolutionary history. In Sahara-Sahel, climatic oscillations shifted the desert extent during the Pliocene-Pleistocene interval, triggering the diversification of several species. Here, we investigated how these biogeographical and ecological events have shaped patterns of genetic diversity and divergence in African Jerboas, desert specialist rodents. We focused on two sister and cryptic species, Jaculus jaculus and J. hirtipes, where we (1) evaluated their genetic differentiation, (2) reconstructed their evolutionary and demographic history; (3) tes…

Increased radiation from Chernobyl decreases the expression of red colouration in natural populations of bank voles (Myodes glareolus)

AbstractPheomelanin is a pink to red version of melanin pigment deposited in skin and hair. Due to its bright colour, pheomelanin plays a crucial function in signalling, in particular sexual signalling. However, production of pheomelanin, as opposed to its dark alternative, eumelanin, bears costs in terms of consumption of antioxidants important for protection of DNA against naturally produced reactive oxidative species. Therefore, decreased expression of pheomelanin is expected in organisms exposed to severe oxidative stress such as that caused by exposure to chronic ionizing radiation. We tested if variable exposure to radiation among natural populations of bank voles Myodes glareolus in …

Repeated evolution of camouflage in speciose desert rodents

AbstractThere are two main factors explaining variation among species and the evolution of characters along phylogeny: adaptive change, including phenotypic and genetic responses to selective pressures, and phylogenetic inertia, or the resemblance between species due to shared phylogenetic history. Phenotype-habitat colour match, a classic Darwinian example of the evolution of camouflage (crypsis), offers the opportunity to test the importance of historical versus ecological mechanisms in shaping phenotypes among phylogenetically closely related taxa. To assess it, we investigated fur (phenotypic data) and habitat (remote sensing data) colourations, along with phylogenetic information, in t…

Supplementary data for article: Camouflage accuracy in Sahara-Sahel desert rodents