Evolution of extreme ontogenetic allometric diversity and heterochrony in pythons, a clade of giant and dwarf snakes

Abstract

Ontogenetic allometry, how species change with size through their lives, and heterochony, a decoupling between shape, size, and age, are major contributors to biological diversity. However, macroevolutionary allometric and heterochronic trends remain poorly understood because previous studies have focused on small groups of closely related species. Here, we focus on testing hypotheses about the evolution of allometry and how allometry and heterochrony drive morphological diversification at the level of an entire species-rich and diverse clade. Pythons are a useful system due to their remarkably diverse and well-adapted phenotypes and extreme size disparity. We collected detailed phenotype data on 40 of the 44 species of python from 1191 specimens. We used a suite of analyses to test for shifts in allometric trajectories that modify morphological diversity. Heterochrony is the main driver of initial divergence within python clades, and shifts in the slopes of allometric trajectories make exploration of novel phenotypes possible later in divergence history. We found that allometric coefficients are highly evolvable and there is an association between ontogenetic allometry and ecology, suggesting that allometry is both labile and adaptive rather than a constraint on possible phenotypes.

The evolution of ontogenetic allometric trajectories in mammalian domestication

“…; Esquerré et al. ), I projected a phylogenetic framework into allometric space to produce a phylomorphospace (sensu Sidlauskas ) using phylomorphospace in the R package phytools version 06–20 (Revell ) and a topological scaffold based on calibrated divergence estimates (Bininda‐Emonds et al. ; O'Leary et al.…”

“…; Wilson ; Esquerré et al. ; Hipsley and Müller ), and have been proposed as pathways for increasing morphological disparity, the quantitative description of the distribution of taxa in morphospace (Foote ). Despite the recognized connection between evolution and development (Raff ; Love ), the role of ontogenetic allometry in shaping patterns of disparity and the utility of ontogenetic allometry as a link between ontogeny and disparity has been underappreciated (Zelditch et al.…”

Prenatal allometric trajectories and the developmental basis of postcranial phenotypic diversity in bats (Chiroptera)

“…Pairwise comparisons of the slope angles (the direction of shape change with size) and lengths (magnitude of shape change with size) were extracted from the HOS, and statistical significance was evaluated using 10,000 iterations. HOS pairwise comparisons that showed parallel allometric trajectories (i.e., did not reject the null hypothesis of common slopes) were then tested for differences in the intercept along the shape axis, with a test for differences in the least square means (Esquerré et al, ; Wilson, ). This test assesses whether different allometric trajectories share the same intercept (H 0 ) or not (H 1 ), and was performed with the advanced.procD.lm function of the R package Geomorph, with 10,000 iterations to assess statistical significance.…”

“…All the tests were performed at the species and subordinal levels. Ontogenetic allometric trajectories were visualized by plotting the first principal component of the predicted values extracted from the shape–size regression against size (Adams & Nistri, ; Esquerré et al, ; Wilson, ). All analyses were performed in R version 3.3.2.…”

“…With this approach, the allometric trajectory of each taxon is represented by a single point in the allometric space. Subsequently, a phylogenetic scaffold was projected into the allometric space to produce a phyloallomspace (Esquerré et al, ) using the phylomorphospace function of the R package phytools version 06‐20 (Revell, ). Phylogenetic relationships and calibrated divergence estimates follow a recent, comprehensive extant bat phylogeny by Shi and Rabosky ().…”