Isolation by Aesop's Fable in NYC mice

Town Mouse Country Mouse
The story goes like this: Town Mouse goes to visit his friend in the country. Town Mouse looks down his long nose at the food offered by Country Mouse, so he brings Country Mouse back to the city for a feast. The food is incredible, but their meal is interrupted by a scary predator. Country Mouse realizes that life in the city, while glamorous and decadent, isn’t worth all the stress.
For Jason Munshi-South and colleagues, it must be fun (or not) to lead off a grant proposal with how you’d like to scientifically test a thousand-year-old fable.

Two new pre-prints available on bioRxiv from Munshi-South and collaborators are using thousands of genetic loci to test how big city life affects the genetic diversity and demographic history of NYC mice.
Isolation by Urbanization
First, Munshi-South and colleagues sampled mice from populations running a gradient of highly-isolated urban environments to lesser-developed suburban and rural sites around New York City. At and around these sites, they calculated the proportion of impervious surface and the size of human populations. After all, what is “suburban” for NYC is likely to be strongly “urban” for other cities. The authors used double-digest RADseq to obtain more than 10,000 loci for 233 individuals in order to understand:

  1. how genome-wide variation relates to urbanization
  2. how urbanization is associated with population structuring
  3. if genetic differentiation is explained by euclidean distance, resistance distance, or ecological distance

All those loci tell quite the story about how urban mice differ from their suburban/rural counterparts. Heterozygosity, nucleotide diversity, percent polymorphic loci, and the number of private alleles were all negatively associated with the percent of impervious surface around populations. Genetic isolation by resistance or by environment were most supported when compared to isolation by distance models, suggesting that the urban landscape/environment played a large part in structuring the observed genetic diversity.

The results presented here demonstrate for the first time that urbanization is associated with a pervasive reduction in genome-wide variation among animal populations.

This may suggest a loss of evolutionary potential in these urban populations but could also be evidence for selective sweeps resultant of strong local adaptation.
Barriers by land, sea, and the human-scape
One outstanding question from the first paper: what is the time frame for all this isolation? Since Europeans began settling NYC in the early 1600s, the idea of what a “green space” is (and what is inviting to white-footed mice) has changed extensively. A mouse might be most comfortable in a cemetery or private garden in 1610, while today’s urban parks might offer a different, but even more isolated, environment.
Stephen Harris led a team of scientists from the City University of New York and Fordham University in using the same SNP dataset from above to test various demographic models of NYC mice.

Can we distinguish recent, human-driven demographic changes from older natural events under a complex model? What natural and anthropogenic barriers drive population divergence in NYC populations? Do population sizes change in response to habitat fragmentation during urbanization? How do human-built barriers to dispersal affect gene flow between urban rodent populations?

Good questions! The answers seem to be: yes, the river/sound and urbanization, yes, and they reduce it. Now you don’t even have to read the paper!
The authors assigned individuals to two main groups separated by the East River and Long Island Sound using sNMF, a result that was confirmed by visualizing population trees made with Treemix. Some of these populations are recently-fragmented and other sites show no signal of admixture whatsoever.
The demographic models most support a historical divide between the two primary groups with subsequent fragmentation that matches the urban isolation of small populations:

Our demographic models estimated divergence times and migration patterns that are consistent with the known geologic and historical record of NYC. This study is the first to use population genomic modeling to estimate the demographic impact of urbanization on wild populations.
 

So, what does high-resolution genetic data tell us about Town Mouse and Country Mouse? It is highly unlikely that Town Mouse made it to dinner in the first place.
 
Cited
Harris, S. E., Xue, A. T., Alvarado-Serrano, D., Boehm, J. T., Joseph, T., Hickerson, M. J., & Munshi-South, J. (2015). Urbanization shapes the demographic history of a city-dwelling native rodent. bioRxiv, 032979.
Munshi-South, J., Zolnik, C. P., & Harris, S. E. (2015). Population genomics of the Anthropocene: urbanization is negatively associated with genome-wide variation in white-footed mouse populations. bioRxiv, 025007.

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