Origins of cryptic coloration in Sand Hills deer mice

On the Origin and Spread of an Adaptive Allele in Deer Mice

Catherine R. Linnen,1* Evan P. Kingsley,1 Jeffrey D. Jensen,2 Hopi E. Hoekstra.1 Science (2009) 325:1095

In this paper, the authors investigated the genetic basis of coat coloration in deer mice (Peromyscus maniculatus) in the Sand Hills of Nebraska.  This particular region is predominately sand dunes, which have a much lighter color than the surrounding soils.  Deer mice in the Sand Hills are also lighter in color (see them below on their non-native, contrasting soil), presumably an adaptation to hide from predators, especially raptors that are highly visual.  Studies done by Dice at U Michigan in the 1930’s and ’40’s with Peromyscus also support this idea that predators (in his experiments, owls) are more likely to eat the mice that stand out against the soil background.

Peromyscus on contrasting soils: left, Sand Hills; right, wildtype. From Linnen et al (2009).

The first set of experiments done in this paper sought to determine what causes the deer mice to have a particular coat color.  What they found is that the coat lightness (measured by reflectance) is strongly correlated with the wide of a light yellow band, caused by pheomelanin pigments, in the hair shaft.  In house mouse, similar banding patterns are a result of a pulse of expression from the Agouti gene, a well-characterized pigmentation gene.  On further investigation by these authors, it is clear that not only is Agouti responsible for the wide band of pheomelanin in the deer mice, but there are regulatory changes in the Sand Hills population that cause Agouti to be expressed longer and at higher levels during hair growth than the ‘outside’ populations.

To determine the exact mutations that lead to the wideband phenotype, the authors sampled from two hybrid populations at the edge of the Sand Hills, and sequenced Agouti for association mapping within the gene.  They identified one significant change, a deletion in exon 2 that results in loss of a serine residue.  This deletion happens to lie in a conserved region of Agouti that interacts with another protein in the pigmentation pathway, Attractin.  The authors suggest three possible conclusions: (1) this serine deletion is directly responsible for the phenotype through its functional interaction with Attractin (2) the deletion is tightly linked to the actual causal mutation, or (3) this deletion is one of a set of tightly linked, coadapted mutations.

The association mapping of the causal mutations here spurred a fair bit of discussion.  While the authors seem to make a big deal of the significant coding change they identified, it was clear that they did not have the resolution to determine that was the actual causal mutation.  Part of this comes from the fact that they sequenced a relatively small region of Agouti, focusing their effort on sequencing the exons, and a small (1kb) region surrounding the significant deletion in exon 2.  Given that these authors presented very clear data showing that differences in Agouti regulation lead to wide pheomelanic bands, I think that they likely missed the key regulatory site that is actually causal.

To wrap up this paper, the authors investigated whether there had been selection for the wide-band phenotype.  Their results clearly demonstrate positive selection acting on the wide band allele.  They further show that this allele arose less than 8000 years ago, sometime after the formation of the Sand Hills geology.  This suggests that the advantageous mutation arose after mice had colonized the Sand Hills.  Maybe a response to pressures such as this….

Red-tailed hawk and prey (Photograph: Steve Jurvetson)

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