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Causes and consequences of seasonal changes in the braincase and brain size of the common shrew Sorex araneus

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Causes and consequences of seasonal changes in the braincase and brain size of the common shrew Sorex araneus

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LAZARO TAPIA, Javier, 2018. Causes and consequences of seasonal changes in the braincase and brain size of the common shrew Sorex araneus [Dissertation]. Konstanz: University of Konstanz

@phdthesis{LazaroTapia2018Cause-42504, title={Causes and consequences of seasonal changes in the braincase and brain size of the common shrew Sorex araneus}, year={2018}, author={Lazaro Tapia, Javier}, address={Konstanz}, school={Universität Konstanz} }

2018-06-07T06:03:14Z Non-migratory animals living in harsh seasonal environments have developed various coping strategies involving seasonal changes in anatomy, physiology and behavior. One of the most outstanding but poorly investigated cases of anatomical seasonal change is the process undergone by several species of red-toothed shrews (subfamily Soricinae), known as Dehnel’s Phenomenon. Extreme reversible seasonal phenotypic variation of skull size, spine length and body mass was first described in the common shrew (Sorex araneus). Offspring are born in late spring/early summer and quickly reach a first size peak at dispersal. Then braincase height – the most frequently used proxy for skull size in the research of this phenomenon – decreases in autumn, reaching a 17–26% smaller minimum in winter. In spring, coinciding with sexual maturation, braincase height increases again by 12–18%, reaching a second peak in the shrews’ second summer. The few surviving post-reproductive individuals then begin a second decline, but die before their second winter. Most organs also decrease in mass toward winter and regrow in early spring. This includes the brain with a 10-26% winter mass decline and 9-16% spring regrowth. These size reductions are hypothesized to reduce energy requirements during winter, with regrowth in spring allowing full exploitation of the only reproductive period in the shrews' life.<br /><br />In my thesis I attempted to answer a series of open questions on Dehnel’s Phenomenon. I studied a population of S. araneus in South Germany. I explored different aspects of the seasonal differences in both skull and brain which involve detailed descriptions of the overall and structural anatomical changes at different levels as well as the consequences of the phenomenon in behavior.<br /><br />First, I wanted to monitor the changes in braincase size at the individual level. To date this shrinkage and regrowth of skull was only described with post mortem measurements of extracted bones and organs, i.e. one measurement per animal. Most authors agree that these data reflect changes within an individual despite collection at population level and are not a result of seasonal selection against large individuals. To exclude the possibility of Dehnel’s Phenomenon being enhanced or even caused by seasonal size biased selection, repeated measures at an individual level were needed. Using time series of x-ray images I showed for first time that in anticipation of winter individual free-ranging shrews shrink their braincases by an average -15.3% (individual maximum -20.1%). Thereafter, during winter and spring, shrews then re-grow their braincases by +9.3% (individual maximum +13.2 %). My results confirm that this variation is thus not caused or enhanced by seasonal size dependent mortality, but reflects profound individual changes in bone anatomy.<br /><br />Second, I attempted to investigate the seasonal changes in brain structure at the regional and cellular levels. I described in detail the volumetric differences between seasons and sexes in particular brain regions, revealing that different regions varied in the magnitude of change. For some regions males and females showed different patterns. Also, I attempted to study the changes in neuron morphology. I observed a general decrease in soma size and total dendrite volume in the caudoputamen and anterior cingulate cortex. This neuronal retraction can partially explain the overall tissue shrinkage in winter which is not sufficient to explain the entire seasonal process, but this represents a first step to understand the underlying drastic transformations in brain tissue.<br /><br />Last, I assessed the changes on skull and brain size at the population level from postmortem samples. Also I wanted to investigate the possible cognitive consequences of the seasonal brain size change. The average decrease in braincase height from July juveniles to February subadults was -12% and the regrowth to adults (June -August) was +13%. I reported a 21% loss of brain mass in winter and 17% re-increase in spring. Additionally, I observed that these changes in turn correlated to the animals' cognitive performance. Search paths of smaller-brained winter individuals in a spatial learning task are longer compared to those of large brained summer juveniles, and spring adults, whose brains have regrown. This implies a trade-off between energetic limitations and cognitive advantages as an adaptation to seasonally fluctuating resources.<br /><br />In conclusion, I attempted to enlighten some of the factors that cause the seasonal changes in the skull and the brain size of the common shrew, as well as its implications in behavior within an ecological-evolutionary framework. This study system can help us to better understand the complex processes that shape the development and evolution of the mammalian skull and brain. But the study of this phenomenon also has great implications in medical research, particularly in investigations related to degenerative processes of bone and brain tissues. terms-of-use Causes and consequences of seasonal changes in the braincase and brain size of the common shrew Sorex araneus 2018-06-07T06:03:14Z 2018 Lazaro Tapia, Javier Lazaro Tapia, Javier eng

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