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.