Dehnel’s phenomenon in other species and general remarks
Sorex araneus is a model species for studies of Dehnel’s Phenomenon. However, it is not the only species showing Dehnel’s Phenomenon and, in fact, not showing the most extreme changes. We found literature on seasonal variation in braincase and/or brain size in 16 mammalian species, including S. araneus (see the species list and data summary in Table S3, Supporting Information). Seven of these species belong to the genus Sorex and 10 of them are shrews (Soricidae ). Sorex minutus exhibits the most profound seasonal changes: its braincase height decreases 19.1% in winter and regrows 15.5% in spring (Kubik, 1951); and brain mass decreases by 34.3% and regrows by 20.3% (Caboń, 1956).
Most species showing Dehnel’s Phenomenon are soricids and small mustelids. They have in common that are small, short-lived predators with high metabolisms, which are unable to use torpor or hibernate and which mostly delay reproduction to the following spring. Thus, Dehnel’s Phenomenon might be a convergent adaptation to winter under similar conditions in these two phylogenetically distant groups (Dechmannet al. , 2017). This is confirmed by observations of decline in braincase and brain size in captive mustelids. Brains of captive ferrets (Mustela putorius ) shrink by 11-19% during 10 months after a postnatal growth peak (Apfelbach & Kruska, 1979; Weiler, 1992). A similar decrease of 14-18% in brain mass was observed in mink from fur farms (Mustela vison ) (Kruska, 1977) here also followed by 17% regrowth in adults (Kruska, 1993). However, we excluded these studies from our species list because the changes were not clearly linked to seasonality, and there is a known overall decreasing effect of domestication on brain size (Kruska, 1993).
We found one additional taxon where seasonal size changes were observed: the morphology of arvicoline voles (Rodentia) also changes seasonally (Yaskin, 1984, 2011, 2013), even though they have a lower metabolic rate than soricids and mustelids, subsist on low quality food and are able to reduce their metabolism in winter. And in fact, we postulate that the change in average size of skull or brain found at the population level in these species does not necessarily reflect individual size changes. Selective mortality of large individuals during summer and autumn can lead to a smaller mean body size in populations of voles and weasels in winter (Szafrańska, Zub, & Konarzewski, 2013; Zub et al. , 2014). In contrast to shrews, which reproduce only in summer, arvicoline voles breed year-round. Variation similar to Dehnel’s Phenomenon could then be caused by seasonal size differences in cohorts, with smaller animals born in autumn and winter, as is the case in some rodents and non-soricine shrews (Schwarz et al. , 1964; Dapson, 1968; Brown, 1973; Markowski & Ostbye, 1992). Confounding Dehnel’s Phenomenon and a seasonal cohort effect in Blarina brevicaudaI wrongly led to reject the existence of the phenomenon (Dapson, 1968). A mean size decrease at population level can also be caused by emigration of large individuals or recruitment of small ones (Iverson & Turner, 1974). A ”decline” caused by any of these processes, might be followed by an increase in mean size, caused by the inverted process or simply by continued individual growth, which then cannot be considered a “re-growth”. Size-corrected analyses of carefully aged individuals, such as in Dechmann et al. (2017), LaPoint et al. (2017) and Lázaro et al. (2018a) are necessary to account for individual size variation and describe relative changes in the size of the brain. The only species for which Dehnel’s Phenomenon in the skull and thus brain has been followed at the individual level is S. araneus (Lázaro et al. , 2017). Mean braincase height of our Southern German population in Radolfzell decreased by 12% between July and February (Lázaro et al. , 2018a). In that same population, recaptured individuals decreased by 15-20% during the same period (Lázaro et al. , 2017),indicating that the estimations at the population level might be biased by the factors mentioned above. Thus, when studying Dehnel’s Phenomenon we must carefully choose the approach and methods.
This also emphasizes that body mass should only be used in combination with other variables to describe Dehnel’s Phenomenon. Individual loss in body mass from summer to winter is common and can have different causes (Zub et al. , 2014). Most often it is simply a consequence of lack of resources in winter. Many species store fat resulting in a weight peak in late summer, followed by a decline along autumn and winter as they use it up. In contrast to the anticipatory shrinking of the shrew, which also includes the skeleton and many major organs, this body mass decrease is therefore not adaptive but a consequence of ambient conditions, which would not occur if resources were still available. Common shrews in captivity reduce food intake during winter and both body mass and braincase height decrease even when provided with foodad libitum (Churchfield, 1982; Lázaro et al. , 2019). The two kinds of body mass changes – as a consequence of current ambient conditions vs. adaptive – are then regulated by different physiological processes, triggered and modulated by different external zeitgebers, and are ultimately the result of different evolutionary drivers (Hyvärinen, 1984). They must be studied under separated theoretical frameworks so as not to be confounded. We suggest that individual changes in skull dimensions and brain mass are the most distinctive features of the morphological changes associated with Dehnel’s Phenomenon. Until the size changes of other organs have been better described for various populations, we recommend using the extracted or scanned skull and brain in combination with body mass to verify and measure Dehnel’s Phenomenon.
As important as choosing the right morphological trait to measure is the correct timing of measurements. Our brain size results from Gugny indicate that choosing the wrong timing may profoundly affect how Dehnel’s Phenomenon is described in a given study. To date, the phenology of Dehnel’s Phenomenon has not been investigated. To the best of our knowledge, based on our own data and the information collected from literature, the time of the year at which each stage of Dehnel’s Phenomenon takes place, may vary between populations and perhaps even between years. In the common shrew the first size peak in the summer juveniles occurs between June and August; the minimum in winter subadults has been reported between December and March; and the second peak, in sexually mature adults, is reached between May and August. The timing at each site may differ. Also, the duration of both decrease and regrowth phases have a strong impact on individuals’ biology, as it determines the rate of tissue shrinkage or regeneration. Viktorov (1967) suggested a possible geographic trend in Dehnel’s Phenomenon phenology: the braincase regrowth phase tends to shorten from western (UK) to eastern (Russia) Europe, in contrast to the rate of regrowth which increases towards eastern populations. Studying the specific timing of each peak and minimum in each population might reveal correlations with current environmental factors and therefore provide more information on the triggers and evolutionary drivers of Dehnel’s Phenomenon. Such added knowledge of the exact timing of the change of each tissue (bone, brain region or organ) in conjunction with studies of gene expression and the detailed mechanisms involved will be important to truly interpret the adaptive value of Dehnel’s Phenomenon. For example, the fact that the brain is largest in young dispersing juveniles and then only partially regrows in reproductive adults, which instead invest in larger body mass suggests that different drivers lead to the shrinking and the regrowth but only a detailed and holistic quantification of the costs and functions of various tissues at each stage will allow us to answer this. Perhaps then, we can understand more general questions, such as why soricine shrews and small mustelids pursue the risky strategy of reproducing only so close to the end of their brief lifespan.