Tail Length Evolution in Deer Mice: Linking Morphology, Behavior, and Function

Abstract

Determining how variation in morphology affects animal performance (and ultimately fitness) is key to understanding the complete process of evolutionary adaptation. Long tails have evolved many times in arboreal and semi-arboreal rodents; in deer mice, long tails have evolved repeatedly in populations occupying forested habit even within a single species (Peromyscus maniculatus). Here we use a combination of functional modeling, laboratory studies, and museum records to test hypotheses about the function of tail-length variation in deer mice. First, we use computational models, informed by museum records documenting natural variation in tail length, to test whether differences in tail morphology between forest and prairie subspecies can influence performance in behavioral contexts relevant for tail use. We find that the deer mouse tail plays little role in statically adjusting center of mass or in correcting body pitch and yaw, but rather it can affect body roll during arboreal locomotion. In this context, we find that even intraspecific tail-length variation could result in substantial differences in how much body rotation results from equivalent tail motions (i.e., tail effectiveness), but the relationship between commonly-used metrics of tail-length variation and effectiveness is non-linear. We further test whether caudal vertebra length, number, and shape are associated with differences in how much the tail can bend to curve around narrow substrates (i.e., tail curvature) and find that, as predicted, the shape of the caudal vertebrae is associated with intervertebral bending angle across taxa. However, although forest and prairie mice typically differ in both the length and number of caudal vertebrae, we do not find evidence that this pattern is the result of a functional trade-off related to tail curvature. Together, these results highlight how even simple models can both generate and exclude hypotheses about the functional consequences of trait variation for organismal-level performance.

Chromosomal inversion polymorphisms shape the genomic landscape of deer mice

“…Furthermore, five inversions (inv7.2, inv14.0, inv15.0, inv18.0, inv21.0) were significantly associated with an ecotype-defining trait, tail length, in laboratory-raised F 2 hybrids 20 (P < 0.05, linear model) and, for all five, the forest arrangement was associated with longer tails (Fig. 6c), consistent with long tails being important for balance in arboreal habitats 36 . These five inversions together explain 23.0% of the variance in tail length (individually explaining 2.0-12.5% of the variance, with additive effects ranging from 1.1-2.7 mm change in tail length).…”

A chromosomal inversion contributes to divergence in multiple traits between deer mouse ecotypes

“…In 1909, Wilfred Osgood described several morphological differences—including tail length and coat color—that distinguish forest and prairie ecotypes of P. maniculatus ( 7 ). Long tails are thought to be beneficial for arboreality ( 8 , 9 , 23 ): Long tails have repeatedly evolved in association with forest habitat in deer mice ( 20 ) and across mammals ( 24 ), and forest mice are better climbers ( 23 ), with tail length differences between the ecotypes likely sufficient to affect climbing performance ( 25 ). Coat color is subject to pressure from visually hunting predators ( 19 ), and many mammals, including deer mice, evolve coats to match local soil color ( 9 , 26 ).…”

Massive inversion polymorphisms shape the genomic landscape of deer mice

“…Specifically, we genotyped the 13 polymorphic inversions in 136 samples across an environmental gradient and found that nine inversions show steep changes in frequency across the forest-prairie habitat transition (Figure 6B, Figure S7), suggesting that these inversions may be favored in alternate habitats. Furthermore, five inversions (inv7.2, inv14.0, inv15.0, inv18.0, inv21.0) are significantly associated with an ecotype-defining trait, tail length, in lab-raised F2 hybrids 19 , and for all five, the forest arrangement is associated with longer tails (Figure 6C), consistent with long tails being important for balance in arboreal habitats 34 . Inv15.0 was also previously found to be significantly associated with coat color, a second ecotype-defining trait 19 (Figure 6C).…”