The Behavioral Consequences and Developmental Genetic Causes of Whisker Evolution in Deer Mice
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Gable, Jacob Taylor
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CitationGable, Jacob Taylor. 2020. The Behavioral Consequences and Developmental Genetic Causes of Whisker Evolution in Deer Mice. Doctoral dissertation, Harvard University, Graduate School of Arts & Sciences.
AbstractIn mammals, whiskers are an important tactile tool, found in all species with the exception of humans. Whiskers, modified hairs with highly innervated follicles, enable individuals to sense and navigate their environment. Thus, different species vary in whisker morphology, from whisker position and number to whisker length, based on their function in different environments – from vibration detection in marine mammals to protective facial reflexes in cats and dogs.
In rodents, while the position and number of whiskers is relatively conserved, there is tremendous variation in the length of whiskers. One observation is that arboreal rodents living in forested environments tend to have longer whiskers than their more terrestrial counterparts. In this dissertation, I examine whisker morphology in two ecologically distinct, but recently diverged, subspecies of the deer mouse, Peromyscus maniculatus, to unravel both the ultimate and proximate mechanisms driving whisker length variation. Specifically, I first aim to understand how differences in whisker length affects an ecologically relevant behavior, and second, how developmental and genetic changes led to the evolution of whisker-length differences.
In Chapter 1, I explore the behavioral effects of differences in whisker length. First, I measured whisker length between forest- and prairie-dwelling deer mice and found that whiskers are on average 41% longer in forest than prairie mice. To determine if these naturally evolved whisker-length differences affects an individual’s ability to detect environmental features, I tested both forest and prairie mice, with trimmed and untrimmed whiskers, in a gap-crossing assay. My results suggest that the longer whiskers of forest mice allow for longer range detection of environmental features than prairie mice, likely an adaptation for an arboreal lifestyle.
In Chapter 2, I measure whisker growth in forest and prairie mice to identify the developmental mechanisms underlying differences in whisker length. I first found that forest and prairie mice grow whiskers at the same rate, but that forest mice grow whiskers for a longer period of time. Second, using whisker-trimming experiments, I show that both subspecies grow whiskers for a specific time period, rather than grow to a specific length. Third, by examining whisker follicle cell proliferation and morphology over time, I found that forest mice have a longer period of anagen (growth phase). This work suggests that developmental changes that extend the whisker growth phase are largely responsible for longer whiskers in forest mice.
In Chapter 3, I combine quantitative trait loci (QTL) mapping and RNA-sequencing to characterize the genetic architecture of whisker length differences and identify candidate genes contributing to this ecologically relevant trait. Using a reciprocal intercross between forest and prairie mice, I localize seven genomic regions contributing to longer whiskers in forest mice, some of which may have specific effects on individual whiskers. Using whisker follicle tissue collected at three time-points during whisker growth in the two subspecies, I identify 14 candidate genes that both occur within QTL regions and show significant expression differences between the subspecies over time. To further narrow the list of candidates, I test for allele-specific expression differences in F1 hybrid whisker follicle tissue. The intersection of these three datasets points to a single candidate TgfBI, a gene involved in TgfB signaling which is implicated in the termination of hair growth, and which shows delayed expression in the long-whiskered forest mice. Future work is aimed at testing the functional role of this gene in evolution of whisker length in deer mice.
Together, my work – integrating measurement of morphology and behavior with developmental and genetic experiments – determines how changes in the genome acts through development to cause the evolution of an important sensory trait, one that affects the ability of an animal to navigate its environment.
Citable link to this pagehttps://nrs.harvard.edu/URN-3:HUL.INSTREPOS:37365854
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