Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study

Abstract

Ecological character displacement describes a pattern where morphological differences between sympatric species are enhanced through interspecific competition. Although widely considered a pervasive force in evolutionary ecology, few clear-cut examples have been documented. Here we report a case of ecological character displacement between two salamander species, Plethodon cinereus and Plethodon hoffmani. Morphology was quantified by using linear measurements and landmark-based geometric morphometric methods for specimens from allopatric and sympatric populations from two geographic transects in south-central Pennsylvania, and stomach contents were assayed to quantify food resource use. Morphological variation was also assessed in 13 additional allopatric populations. In both transects, we found significant morphological differentiation between sympatric populations that was associated with a reduction in prey consumption in sympatry and a segregation of prey according to prey size. No trophic morphological or resource use differences were found between allopatric populations, and comparisons of sympatric populations with randomly paired allopatric populations revealed that the observed sympatric morphological differentiation was greater than expected by chance. The major trophic anatomical differences between sympatric populations relates to functional and biomechanical differences in jaw closure: sympatric P. hoffmani have a faster closing jaw, whereas sympatric P. cinereus have a slower, stronger jaw. Because salamanders immobilize prey of different sizes in different ways, and because the observed sympatric biomechanical differences in jaw closure are associated with the differences in prey consumption, the observed character displacement has a functional ecological correlate, and we can link changes in form with changes in function in this apparent example of character displacement.

Figure 1

Positions of 13 landmarks used in this study. All landmarks were digitized from the left-lateral view of the skull (modified from Adams, ref. 14).

Figure 2

(A) Mean values of morphological characters for P. cinereus and P. hoffmani in sympatry and allopatry for both the eastern geographic transect (Fulton County, PA) and the western geographic transect (Bedford and Somerset Counties, PA). Population labels are as follows: ah, allopatric P. hoffmani; sh, sympatric P. hoffmani; sc, sympatric P. cinereus; and ac, allopatric P. cinereus. (B) Plot of the first two axes from a canonical variates analysis of head shape (using ratios on SVL), showing the significant sympatric differentiation of size-adjusted head shape (Wilks' Λ = 0.184, F = 18.91, P = 1.8 × 10⁻⁴³). (C) Histograms showing the distributions of morphological differences between randomly paired allopatric populations relative to the observed sympatric differentiation for both the eastern (Fulton County) and western (Bedford and Somerset Counties) transects. (D) Profiles of resource use for sympatric populations. The 16 prey categories are sorted according to size and show the significant segregation of resources (Fulton County data from Adams, ref. 15).

Figure 3

(A and B) Thin-plate spline representations of the average specimen from sympatric P. cinereus and sympatric P. hoffmani, allowing visualization of the significant differences in head shape (Wilks' Λ = 0.0513, F = 10.68, P = 2.99 × 10⁻⁵⁴), where the sympatric divergence (Mahalanobis generalized distance) was statistically greater than the allopatric divergence (randomization test; P_rand = 0.02). The observed sympatric differences have been exaggerated by a factor of 2. (C) Multivariate association for sympatric specimens of trophic morphology as represented by geometric shape variables and food resource use (square root of the number of prey consumed per prey category) from a two-block partial least-squares analysis (r = 0.7591, P_rand = 0.001). The x axis represents morphology (extremes illustrated by using a thin-plate spline), and the y axis represents food resource use (positive values = large prey; negative values = small prey).

Figure 4

(A) Biomechanical representation of jaw closing mechanism. The squamosal is represented as the in-lever (l_i), and the dentary is represented as the out-lever (l_o). (B) Plot of ratios of squamosal length to dentary length.