Profound seasonal shrinking and regrowth of the ossified braincase in phylogenetically distant mammals with similar life histories

Dina K N Dechmann,Scott Lapoint,Martin Wikelski,Karol Zub,Jan R E Taylor,Christian Dullin,Moritz Hertel

doi:10.1038/srep42443

Abstract

Ontogenetic changes in skull shape and size are ubiquitous in altricial vertebrates, but typically unidirectional and minimal in full-grown animals. Red-toothed shrews exhibit a rare exception, where the shape, mass and size of the skull, brain, and several major organs, show significant bidirectional seasonal changes. We now show a similar but male-biased shrinking (16%) and regrowth (8%) in the standardized braincase depth of least weasels (Mustela nivalis). Juvenile weasels also exhibit a growth overshoot, followed by a shrinkage period lasting until the end of their first winter. Only male weasels then regrow during their second summer. High-resolution CT scans suggest areas of the skull are affected differently during shrinking and regrowth in both species. This suggests multiple evolutionary drivers: while the shrinking likely facilitates survival during seasonal low resource availability in these high-metabolic mammals with year-round activity, the regrowth may be most strongly influenced by high investment into reproduction and territories, which is male-biased in the weasels. Our data provide evidence for convergent evolution of skull and thus brain shrinkage and regrowth, with important implications for understanding adaptations to changing environments and for applied research on the correlated changes in bone structure, brain size and the many other affected organs.

Highlights

If these changes are adaptive and driven by seasonal changes, as the tight link of the size extremes to winter and spring indicates, they should manifest in more than one taxon
Weasels and red-toothed shrews diverged during the paleocene[15], yet share several life history traits, including: (i) small size, (ii) limited ability to compensate for heat loss[16,17], (iii) an extremely high metabolism that is always near the maximum[17,18], resulting in constant requirements for high quality food[19], (iv) a short lifespan[19], and (v) year-round activity[17,20] without the ability to optimize energy use through torpor
The magnitude of relative braincase decrease and regrowth that we report here was previously only documented in S. araneus and for the first time in M. nivalis

Summary

Introduction

If these changes are adaptive and driven by seasonal changes, as the tight link of the size extremes to winter (smallest size) and spring (regrowth) indicates, they should manifest in more than one taxon. We quantified seasonal changes in skull length and braincase depth, a common measure for detecting seasonal size change in shrews, in the least weasel, one of the mustelid species that shows a juvenile skull size overshoot similar to juvenile shrews.

Results

Conclusion