Domestication effect of reduced brain size is reverted when mink become feral.

A typical consequence of breeding animal species for domestication is a reduction in relative brain size. When domesticated animals escape from captivity and establish feral populations, the larger brain of the wild phenotype is usually not regained. In the American mink (Neovison vison), we found an exception to this rule. We confirmed the previously described reduction in relative braincase size and volume compared to their wild North American ancestors in mink bred for their fur in Poland, in a dataset of 292 skulls. We then also found a significant regrowth of these measures in well-established feral populations in Poland. Closely related, small mustelids are known for seasonal reversible changes in skull and brain size. It seems that these small mustelids are able to regain the brain size, which is adaptive for living in the wild, and flexibly respond to selection accordingly.

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.

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 Bialowieza 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.

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.

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

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.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.We analyzed the effect of geographic and climate variables on the intensity of change and patterns of brain re-organization.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.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.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.

Metabolic rate in common shrews is unaffected by temperature, leading to lower energetic costs through seasonal size reduction.

Small endothermic mammals have high metabolisms, particularly at cold temperatures. In the light of this, some species have evolved a seemingly illogical strategy: they reduce the size of the brain and several organs to become even smaller in winter. To test how this morphological strategy affects energy consumption across seasonally shifting ambient temperatures, we measured oxygen consumption and behaviour in the three seasonal phenotypes of the common shrew (Sorex araneus), which differ in size by about 20%. Body mass was the main driver of oxygen consumption, not the reduction of metabolically expensive brain mass. Against our expectations, we found no change in relative oxygen consumption with low ambient temperature. Thus, smaller body size in winter resulted in significant absolute energy savings. This finding could only partly be explained by an increase of lower cost behaviours in the activity budgets. Our findings highlight that these shrews manage to avoid one of the most fundamental and intuitive rules of ecology, allowing them to subsist with lower resource availability and successfully survive the harsh conditions of winter.

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.

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.

Small increases in corticosterone before the breeding season increase parental investment but not fitness in a wild passerine bird.

Correlative evidence from field studies has suggested that baseline concentrations of corticosterone, the main avian glucocorticoid hormone, affect reproductive strategies in vertebrate species. Such a role is conceivable in light of corticosterone's function as a metabolic hormone in regulating glucose and fat metabolism. From such correlational studies, however, the question has remained open whether glucocorticoid concentrations change in advance of reproductive activities or whether corticosterone concentrations vary passively as a consequence of the individual's reproductive investment and workload. To test such causal relationships, we manipulated corticosterone concentrations prior to the breeding season in adult great tits (Parus major) and quantified reproductive investment and success. Two weeks before egg-laying, we administered subcutaneous silastic implants filled with corticosterone that elevated circulating levels within the baseline range for approximately 30 days to adult males and females. Corticosterone manipulation did not affect lay date or yearly offspring production. However, reproductive behaviors were affected by corticosterone treatment: males fed their mates more often during incubation, and females increased incubation of eggs and brooding of nestlings compared to control individuals. Other behaviors during the nestling stage, when the implants were no longer effective, did not differ between the two treatment groups. Our findings do not support the view that baseline corticosterone concentrations, at least at the time of year when we administered implants, change reproductive strategies per se. The current data suggest that baseline corticosterone levels represent internal signals that causally mediate reproductive effort in individuals of a wild bird species. By increasing reproductive investment, baseline corticosterone concentrations may have functions during the breeding season that diverge from the suppressive effects of stress-induced concentrations.