Seasonal reversible size changes in the braincase and mass of common shrews are flexibly modified by environmental conditions

Abstract

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.

Seasonal plasticity in the adult somatosensory cortex

“…Animals can show remarkable adaptations to combat adverse conditions ( 28 , 29 ), despite the absence of explicit external cues ( 2 ). In nature, when such adaptations occur together with other triggers like food, photoperiod, and temperature variations, which can induce further acclimatization ( 15 ), the overall effect could be even larger ( 11 ). In the laboratory, even in the absence of direct seasonal cues, the shrews might inherit temporal cues through changes in odors of their prey, as has been observed in other species ( 30 ) or evolved endogenous annual timekeeping mechanisms ( 2 , 31 ).…”

“…Some of the most drastic yet largely unexplored seasonal changes in brain structure have been observed in small mammals, like shrews and weasels ( 11 , 12 ). This phenomenon is known as Dehnel’s effect and entails a reduction in body weight, skull, and brain size during autumn and winter ( 11 – 15 ). We explore this effect in Etruscan shrews and find that individual shrews exhibit seasonal changes in brain size, with the cerebral cortex shrinking in winter.…”

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

“…Common shrews in captivity reduce food intake during winter and both body mass and braincase height decrease even when provided with food ad libitum (Churchfield, 1982;Lázaro et al, 2019).…”

“…However, temperature is also important, at least as a modulator as captive shrews kept at constant temperature cease to express the cycle (Lázaro et al, 2019). However, Dehnel's Phenomenon can differ greatly between populations.…”

Phenotypic Switching Resulting From Developmental Plasticity: Fixed or Reversible?

“…Having made a case for reversible (correctable) phenotype switching enabled by developmental phenotypic plasticity, what might we speculate to be the selection pressures leading to its evolution? Advantages to mature organisms of reversible phenotype switching, as well as its evolution, have received considerable attention -for an entry into the literature see Gabriel (2005), Gabriel (2006), Piersma and van Gils (2010), Berman (2016), Chen et al (2016), Pfab et al (2016), Lazaro et al (2019), and Ratikainen and Kokko (2019). Yet, as Beaman et al (2016) state, ".…”