INTRODUCTION
The adaptive value of phenotypic traits can be identified only when
functional correlations with environmental variables are considered. The
variation of the phenotypes between populations and individuals is often
used to address this. However, individual phenotypic flexibility, where
the adult phenotype can still be modified in response to environmental
change, can be hidden by this approach (Piersma & Drent, 2003). A
special case of such phenotypic change is life-stage cycling, i.e.
seasonal changes along the lifetime of individuals that are reversible.
Studying life-stage cycling allows inferring mechanisms of adaptation to
the environment as the changes are well marked and predictable.
An outstanding case of seasonal phenotypic flexibility are the drastic
but reversible morphological changes called Dehnel’s Phenomenon,
observed in some small, short-lived mammals with high metabolic rates.
In this phenomenon young animals reach a first maximum size in their
first summer, followed by a size decline reaching a minimum size in
winter, They then regrow in the spring along with sexual maturation.
Best studied in the common shrew (Sorex araneus ), Dehnel’s
Phenomenon entails a decrease in overall size, the size of the skull and
other parts of the skeleton, but also the brain and many other organs
and tissues, followed by regrowth (Dehnel, 1949; Pucek, 1965). Brain
mass, for example, decreases by up to 30% from summer to winter and
increases again by 10-17% during the next spring and summer (Bielak &
Pucek, 1960; Lázaro et al. , 2018a). Braincase height, often used
as a proxy for braincase size, decreases by up to 18% and regrows by up
to 15% (Crowcroft & Ingles, 1959; Homolka, 1980; Yaskin, 1994).
Importantly, Dehnel’s Phenomenon causes not just a rescaling of the
animal, but each organ and even each brain region shows a unique pattern
of the direction and magnitude of changes, resulting in several
completely different phenotypes along the year (Yaskin, 1994; Lázaroet al. , 2018b). Also the length of the spine decreases and
regrows seasonally as a result of shrinkage of the inter-vertebral disks
(Saure & Hyvärinen, 1965; Hyvarinen, 1969). Some other species of
shrews, and, as has recently been found, some mustelids, also show
seasonal reversible shrinkage and regrowth at least of their skulls and
brains (Dechmann et al. , 2017; LaPoint et al. , 2017).
Species known to exhibit Dehnel’s Phenomenon are small short-lived
predators with very high metabolic rates, which do not hibernate or
migrate during winter (Taylor, 1998; Ochocińska & Taylor, 2005). They
remain active and dependent on high quality food year-round and the
reversible changes of body and brain are hypothesized to be a winter
adaptation to save energy (Mezhzherin, 1964; Pucek, 1970; Yaskin, 2011).
While direct evidence of a link between the changes in overall size or
specific organs such as the brain and individual survival is still
lacking, reducing metabolically expensive organs, including the brain
during winter, is thought to decrease overall energetic needs and thus
food intake (Churchfield, 1982; Schaeffer et al. , 2020). This
would then compensate for the disadvantages of being small, such as an
increasingly unfavorable volume to surface ratio in winter (Bergmann
1848; Yom-Tov & Yom-Tov, 2005). In support of this, mass corrected
energy consumption remains constant across seasons despite large
differences in ambient temperature, which means overall energy use and
thus food requirements of the size-decreased subadult winter shrews is
lower than in the juvenile summer animals and especially in the adult
individuals, whose mass doubles in the spring (Gębczyński, 1965; Taylor,
Rychlik, & Churchfield, 2013; Schaeffer et al. , 2020). In
addition, although this seasonal cycle occurs in every free-ranging
individual (Lázaro et al. , 2017), the intensity of the size
changes is exceptionally flexible. Captive shrews differ in the
magnitude of seasonal change of skull size when ambient temperature is
manipulated (Lázaro et al. , 2019).
Ambient conditions thus play an important role for Dehnel’s Phenomenon,
but whether as triggers or evolutionary drivers or both, remains
unclear. Braincase changes associated with Dehnel’s Phenomenon in
weasels (Mustela erminea and M. nivalis ) vary greatly in
intensity and timing between populations at different geographic
locations (LaPoint et al. , 2017). Previous studies on common
shrews suggested a greater winter decrease in skull and body size in
Northeastern Europe compared to Southwestern populations (Pucek, 1970;
Spitzenberger, 2001). Similarly, the reorganization of brain structure
differs greatly between two populations in Radolfzell (Southern Germany,
Lázaro et al. 2018b) and Russia (Yaskin, 1994). This increase in the
extent of seasonal size change from regions with milder winter
conditions to regions with harsher winter conditions supports the
hypothesis that Dehnel’s Phenomenon is a winter adaptation. In fact,
this trend towards lower body size when facing harsh conditions also
fits well to the contradictive morpho-geographical patterns observed inSorex shrews. Some Sorex species show lower body size at
higher latitudes (Ochocińska & Taylor, 2003), again contradicting
Bergmann’s rule that predicts larger bodies in colder climates to
increase heat-preservation efficiency (Bergmann 1848, but see Zeveloff
& Boyce 1988). Several small mammal species follow a ‘resource rule’
where body size is directly predicted by resource availability (McNab,
2010). This would explain why common shrews decrease body size in
winter, and predicts a more pronounced summer to winter shrinkage in
environments with harsher winters – at high latitudes. However, a
review of latitudinal differences in seasonal body mass decline did not
find any significant trend (Ochocińska & Taylor, 2003).
We compiled all published work on Dehnel’s Phenomenon, discuss progress
made since the last literature review in 1970 (Pucek, 1970) and take
advantage of the larger currently available dataset to tatistically test
for the influence of geographic and climatic variables on the magnitude
of Dehnel’s Phenomenon in S. araneus . We collected information
from those studies which include changes in skull size and/or brain
mass. From these studies, we also collected total body mass when
reported and explored correlations of the intensity of Dehnel’s
Phenomenon with climatic and geographic variables. We added our own data
on braincase size, brain mass and body mass from new populations in
Poland and body mass and braincase size from the Czech Republic to this
dataset. We expected to find increasing strength of Dehnel’s Phenomenon
along geographical gradient that fits increasingly harsh environmental
conditions related to seasonality, as predicted by previous authors. In
addition, we compiled information on Dehnel’s Phenomenon in other
species and compared their results with S. araneus . Finally, we
specifically investigated the variation in the structural changes within
the brain associated with Dehnel’s Phenomenon between populations. We
compared the divergent results from southern Germany (Lázaro et
al. , 2018b) and Russia (Yaskin, 1994) with new data from a population
in Northeastern Poland, situated geographically between these two. We
expected to find intermediate values of structural change that would fit
into a gradual, geographic pattern in this Polish population. The aim of
this review is to establish an updated framework to study the
evolutionary aspects of this fascinating phenomenon.