Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae)

Abstract

Background: A major goal in evolutionary biology is to understand the evolution of phenotypic diversity. Both natural and sexual selection play a large role in generating phenotypic adaptations, with biomechanical requirements and developmental mechanisms mediating patterns of phenotypic evolution. For many traits, the relative importance of selective and developmental components remains understudied.

Results: We investigated ontogenetic trajectories of foot morphology in the eight species of European plethodontid cave salamander to test the hypothesis that adult foot morphology was adapted for climbing. Using geometric morphometrics and other approaches, we found that developmental patterns in five species displayed little morphological change during growth (isometry), where the extensive interdigital webbing in adults was best explained as the retention of the juvenile morphological state. By contrast, three species exhibited significant allometry, with an increase in interdigital webbing during growth. Phylogenetic analyses revealed that multiple evolutionary transitions between isometry and allometry of foot webbing have occurred in this lineage. Allometric parameters of foot growth were most similar to those of a tropical species previously shown to be adapted for climbing. Finally, interspecific variation in adult foot morphology was significantly reduced as compared to variation among juveniles, indicating that ontogenetic convergence had resulted in a common adult foot morphology across species.

Conclusions: The results presented here provide evidence of a complex history of phenotypic evolution in this clade. The common adult phenotype exhibited among species reveals that selection plays an important part in generating patterns of foot diversity in the group. However, developmental trajectories arriving at this common morphology are distinct; with some species displaying developmental stasis (isometry), while others show an increase in foot webbing during growth. Thus, multiple developmental solutions exist to the same evolutionary challenge. Our findings underscore the importance of examining morphological adaptations from multiple perspectives, and emphasize that both selective hypotheses and developmental processes must be considered for a more comprehensive understanding of phenotypic evolution.

Figure 1

A) Geographic distributions of all species of European Hydromantes; B) Measurements used to characterize foot morphology; C) photo of Hydromantes (S.) strinatii (courtesy of S. Vanni). Foot morphology in European Hydromantes was quantified in several ways, following [27]: 1) foot shape, as defined by the positions of nine anatomical landmarks (numbered), 2) the degree of foot webbing, found as the ratio between the perimeter of the foot (p) divided by foot width (d), 3) foot area (A) enclosed by the outline of the entire foot. The species examined in this study are: H. (S.) ambrosii, H. (S.) flavus, H. (S.) genei, H. (S.) imperialis, H. (S.) italicus, H. (S.) sarrabusensis, H. (S.) strinatii, and H. (S.) supramontis.

Figure 2

Measures of foot morphology as a function of size for all species of European Hydromantes. A) Foot sinuosity versus foot length, B) Predicted values of foot sinuosity ($\widehat{Y}$) from species-specific regressions versus foot length, C) Regression scores of foot shape [46] versus log(Centroid Size), D) Predicted values of foot shape ($\widehat{Y}$) from species-specific regressions versus log(Centroid Size). In all panels, symbol size is proportional to specimen size. Species displaying allometric relationships are shown as circles, while species displaying isometric relationships are shown as diamonds. Species are shown in the following colors: H. (S.) ambrosii = violet; H. (S.) flavus = yellow; H. (S.) genei = beige; H. (S.) imperialis = light green; H. (S.) italicus = light gray; H. (S.) sarrabusensis = red; H. (S.) strinatii = salmon; H. (S.) supramontis = blue.

Figure 3

Thin-plate spline deformation grids depicting foot shape for A) small and B) large individuals. Grids are accentuated by a factor of two to facilitate visual interpretation.

Figure 4

Phylogenetic relationships for all species of European Hydromantes. Relationships based on a molecular phylogeny found from combined mitochondrial and nuclear DNA sequence data, with branch lengths proportional to nucleotide differences [28]. Observed patterns of foot allometry (Figure 2B) are denoted on the phylogeny, along with hypothesized evolutionary transitions found from maximum likelihood ancestral state reconstruction.