EECG Embarkation: Genetics of a unique wintering strategy in Sorex araneus

Posted on November 8, 2022May 30, 2022

**The AGA grants EECG Research Awards each year to graduate students and post-doctoral researchers who are at a critical point in their research, where additional funds would allow them to conclude their research project and prepare it for publication. EECG awardees also get the opportunity to hone their science communication and write posts over their grant tenure for the AGA Blog. In the first in the series, our EECG awardees write about their research and their interests as an ’embarkation’.**

About the Blog Author: Bill Thomas is a PhD candidate in Dr. Liliana Dávalos’ lab at Stony Brook University. My research focuses on uncovering the molecular mechanisms and evolutionary processes of adaptations, where I use a variety of methodologies, such as comparative and population genomics. As I state on my website, I honestly feel quite like Darwin being dropped off by the Beagle on the coast of South America, except my Mac drops me off to explore the vast “-omics” data generated in the past couple of decades to conduct my experiments.

Many of us have likely heard or read Theodosius Dobzhansky’s famous quote, “Nothing in biology makes sense except in the light of evolution” (Dobzhansky 1973). Similar to the arguments Charles Darwin made in “On the Origin of Species” (Darwin 1859), these texts state the diversity of traits found in organisms are only logical if observed through the lens of adaptations to external selective pressures. I often think about these works as I research a unique wintering strategy known as Dehnel’s phenomenon. This strategy is an adaptation in the common shrew, Sorex araneus, where they drastically shrink many of their organs in the fall, with extensive changes in the brain and liver, reaching a minimum during the winter, with rapid tissue regrowth in the spring (Lázaro 2019) (Figure 1). This trait at first glance doesn’t “make sense” as 1) only two typical strategies have commonly evolved for smaller mammals; many migrate to avoid harsh conditions, while others will hibernate, and 2) brains rarely shrink and then regrow, as brain development is a highly conserved process with limited neurogenesis in adulthood (Bartkowska 2008). However, despite the use of shrews as a model of speciation over the past 50 years (Searle 2019), little has been done to make this phenotype “make sense”, thus, I use some of the same methods as Darwin; comparisons between species, observation of development, and biogeography to better understand the molecular mechanisms and evolutionary processes of Dehnel’s phenomenon.

Our current hypothesis is that these shrews shrink through winter to reduce the energy requirements of maintaining large and energetically expensive tissue. We think that metabolism is one of these Darwinian selective pressures paving the way for this adaptation, as shrews have an extremely high metabolism than expected for their body size (Taylor 1998). Thus, in the first two phases of my research, I utilized genomic and transcriptomic data to test this hypothesis. First, I tested whether gene pathways associated with cold adaptation, such as metabolism and thermogenesis, were significantly enriched with genes under positive selection. To do this, I ran branch-site models to test for positive selection in the S. araneus lineage, with initial results showing that genes involved phospholipid metabolism, including genes involved in the human neurodegenerative diseases Alzheimer’s and Parkinson’s, are under positive selection, which may be associated with lipid reduction that occurs in tissue during Dehnel’s phenomenon. This result is validated through my functional experiments, as differential gene expression analyses suggest cholesterol metabolism and movement of high-density lipids regulate shrinkage and regrowth in the brain.

So how will support from the EECG help identify the evolutionary processes that have shaped this adaptation? Much like the natural variation Darwin observed within species that helped shape his theory of natural selection, previous scientists have identified population-level divergence in Dehnel’s phenomenon between subpopulations of shrews, with those in the northeast having greater size reductions (Pucek 1970). This suggests that Dehnel’s phenomenon is locally adapted allowing these shrews to inhabit a wide range of environments with harsh winter conditions. Funds will allow me to produce high coverage genomes of several individuals across the range of phenotype. In tandem with my low coverage genomes of ~100 individuals, I can model both selection and demographic history simultaneously, such that I can infer which genes are under selection and may have played an important role in the evolution of this unique wintering strategy!