Histological and MRI brain atlas of the common shrew, Sorex araneus, with brain region-specific gene expression profiles

The common shrew, Sorex araneus, is a small mammal of growing interest in neuroscience research, as it exhibits dramatic and reversible seasonal changes in individual brain size and organization (a process known as Dehnel’s phenomenon). Despite decades of studies on this system, the mechanisms behind the structural changes during Dehnel’s phenomenon are not yet understood. To resolve these questions and foster research on this unique species, we present the first combined histological, magnetic resonance imaging (MRI), and transcriptomic atlas of the common shrew brain. Our integrated morphometric brain atlas provides easily obtainable and comparable anatomic structures, while transcriptomic mapping identified distinct expression profiles across most brain regions. These results suggest that high-resolution morphological and genetic research is pivotal for elucidating the mechanisms underlying Dehnel’s phenomenon while providing a communal resource for continued research on a model of natural mammalian regeneration. Morphometric and NCBI Sequencing Read Archive are available at https://doi.org/10.17617/3.HVW8ZN

Seasonal reversible size changes in the braincase and mass of common shrews are flexibly modified by environmental conditions

The growth of the vertebrate skull and brain is usually unidirectional and more or less stops when animals are adult. Red-toothed shrews break this rule. They seasonally shrink and regrow brain and skull size by 20% or more, presumably to save energy when conditions are harsh. The size change is anticipatory of environmental change and occurs in all individuals, but it is unknown whether its extent can be modulated by environmental conditions. We kept shrews under different conditions, monitored seasonal changes in skull size with series of X-rays, and compared them with free ranging animals. We found extensive differences in the pattern of skull size change between experimental groups. Skull size of shrews kept at constant temperature showed a steady decline, while the skull size changes of free ranging shrews and captive individuals exposed to natural temperature regimes were identical. In contrast, body mass never reached the spring values of free ranging shrews in either captive regime. The extent of this adaptive seasonal pattern can thus be flexibly adapted to current environmental conditions. Combining reversible size changes with such strong phenotypic plasticity may allow these small, non-hibernating predators with high metabolic rates to continue being successful in today's changing environments.publishe

Winter conditions, not resource availability alone, may drive reversible seasonal skull size changes in moles

Seasonal changes in the environment can lead to astonishing adaptations. A few small mammals with exceptionally high metabolisms have evolved a particularly extreme strategy: they shrink before winter and regrow in spring, including changes of greater than 20% in skull and brain size. Whether this process is an adaptation to seasonal climates, resource availability or both remains unclear. We show that European moles (Talpa europaea) also decrease skull size in winter. As resources for closely related Iberian moles (Talpa occidentalis) are lowest in summer, we predicted they should shift the timing of size changes. Instead, they do not change size at all. We conclude that in moles, seasonal decrease and regrowth of skull size is an adaptation to winter climate and not to a changing resource landscape alone. We not only describe this phenomenon in yet another taxon, but take an important step towards a better understanding of this enigmatic cycle.publishe

Profound seasonal changes in brain size and architecture in the common shrew

The seasonal changes in brain size of some shrews represent the most drastic reversible transformation in the mammalian central nervous system known to date. Brain mass decreases 10-26% from summer to winter and regrows 9-16% in spring, but the underlying structural changes at the cellular level are not yet understood. Here, we describe the volumetric differences in brain structures between seasons and sexes of the common shrew (Sorex araneus) in detail, confirming that changes in different brain regions vary in the magnitude of change. Notably, shrews show a decrease in hypothalamus, thalamus, and hippocampal volume and later regrowth in spring, whereas neocortex and striatum volumes decrease in winter and do not recover in size. For some regions, males and females showed different patterns of seasonal change from each other. We also analyzed the underlying changes in neuron morphology. We observed a general decrease in soma size and total dendrite volume in the caudoputamen and anterior cingulate cortex. This neuronal retraction may partially explain the overall tissue shrinkage in winter. While not sufficient to explain the entire seasonal process, it represents a first step toward understanding the mechanisms beneath this remarkable phenomenon.publishe

Fifty years of data show the effects of climate on overall skull size and the extent of seasonal reversible skull size changes (Dehnel's phenomenon) in the common shrew

Global climate change affects many aspects of biology and has been shown to cause body size changes in animals. However, suitable datasets allowing the analysis of long-term relationships between body size, climate, and its effects are rare. The size of the skull is often used as a proxy for overall body size. Skull size does not change much in fully grown vertebrates; however, some high-metabolic small mammals shrink in winter and regrow in spring, including their skull and brain. This is thought to be a winter adaptation, as a smaller brain size reduces energy requirements. Climate could thus affect not only the overall size but also the pattern of the size change, that is, Dehnel's phenomenon, in these animals. We assessed the impact of the changes in climate on the overall skull size and the different stages of Dehnel's phenomenon in skulls of the common shrew, Sorex araneus, collected over 50 years in the Białowieża Forest, E Poland. Overall skull size decreased, along with increasing temperatures and decreasing soil moisture, which affected the availability of the shrews' main food source, earthworms. The skulls of males were larger than those of females, but the degree of the decrease in size did not differ between sexes. The magnitude of Dehnel's phenomenon increased over time, indicating an increasing selection pressure on animals in winter. Overall, climate clearly affected the common shrew's overall size as well as its seasonal size changes. With the current acceleration in climate change, the effects on the populations of this cold-adapted species may be quite severe in a large part of its distribution range.publishe

Geographic patterns in seasonal changes of body mass, skull, and brain size of common shrews

1. Some small mammals exhibit Dehnel's Phenomenon, a drastic decrease in body mass, braincase, and brain size from summer to winter, followed by a regrowth in spring. This is accompanied by a re‐organization of the brain and changes in other organs. The evolutionary link between these changes and seasonality remains unclear, although the intensity of change varies between locations as the phenomenon is thought to lead to energy savings during winter.2. Here we explored geographic variation of the intensity of Dehnel's Phenomenon in Sorex araneus. We compiled literature on seasonal changes in braincase size, brain, and body mass, supplemented by our own data from Poland, Germany, and Czech Republic.3. We analyzed the effect of geographic and climate variables on the intensity of change and patterns of brain re‐organization.4. From summer to winter, the braincase height decreased by 13%, followed by 10% regrowth in spring. For body mass, the changes were −21%/+82%, respectively. Changes increased toward northeast. Several climate variables were correlated with these transformations, confirming a link of the intensity of the changes with environmental conditions. This relationship differed for the decrease versus regrowth, suggesting that they may have evolved under different selective pressures.5. We found no geographic trends explaining variability in the brain mass changes although they were similar (−21%/+10%) to those of the braincase size. Underlying patterns of change in brain organization in northeastern Poland were almost identical to the pattern observed in southern Germany. This indicates that local habitat characteristics may play a more important role in determining brain structure than broad scale geographic conditions.6. We discuss the techniques and criteria used for studying this phenomenon, as well as its potential presence in other taxa and the importance of distinguishing it from other kinds of seasonal variation.publishe

The effect of improved rural sanitation on diarrhoea and helminth infection: design of a cluster-randomized trial in Orissa, India.

UNLABELLED: BACKGROUND: Infectious diseases associated with poor sanitation such as diarrhoea, intestinal worms, trachoma and lymphatic filariasis continue to cause a large disease burden in low income settings and contribute substantially to child mortality and morbidity. Obtaining health impact data for rural sanitation campaigns poses a number of methodological challenges. Here we describe the design of a village-level cluster-randomised trial in the state of Orissa, India to evaluate the impact of an ongoing rural sanitation campaign conducted under the umbrella of India's Total Sanitation Campaign (TSC).We randomised 50 villages to the intervention and 50 villages to control. In the intervention villages the implementing non-governmental organisations conducted community mobilisation and latrine construction with subsidies given to poor families. Control villages receive no intervention. Outcome measures include (1) diarrhoea in children under 5 and in all ages, (2) soil-transmitted helminth infections, (3) anthropometric measures, (4) water quality, (5) number of insect vectors (flies, mosquitoes), (6) exposure to faecal pathogens in the environment. In addition we are conducting process documentation (latrine construction and use, intervention reach), cost and cost-effectiveness analyses, spatial analyses and qualitative research on gender and water use for sanitation. RESULTS: Randomisation resulted in an acceptable balance between trial arms. The sample size requirements appear to be met for the main study outcomes. Delays in intervention roll-out caused logistical problems especially for the planning of health outcome follow-up surveys. Latrine coverage at the end of the construction period (55%) remained below the target of 70%, a result that may, however, be in line with many other TSC intervention areas in India. CONCLUSION: We discuss a number of methodological problems encountered thus far in this study that may be typical for sanitation trials. Nevertheless, it is expected that the trial procedures will allow measuring the effectiveness of a typical rural sanitation campaign, with sufficient accuracy and validity

Histological and MRI brain atlas of the common shrew, Sorex araneus, with brain region-specific gene expression profiles

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