1. Evolutionary Biology
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Plasticity and evolutionary convergence in the locomotor skeleton of Greater Antillean Anolis lizards

  1. Nathalie Feiner  Is a corresponding author
  2. Illiam SC Jackson
  3. Kirke L Munch
  4. Reinder Radersma
  5. Tobias Uller
  1. Department of Biology, Lund University, Sweden
  2. School of Biological Sciences, University of Tasmania, Australia
Research Article
Cite this article as: eLife 2020;9:e57468 doi: 10.7554/eLife.57468
4 figures and 4 additional files

Figures

Distribution of ecomorphs on the four main Greater Antillean islands and elements of the morphological dataset capturing variation in the locomotor skeleton.

(A) The four islands of the Greater Antilles, Cuba, Jamaica, Hispaniola and Puerto Rico, each inhabit a set of independently evolved ecomorphs (Poe et al., 2017). Colour-coded squares show the number of species that were used in this study. Note that Jamaica and Puerto Rico do not possess the full set of six ecomorphs, but lack one and two ecomorphs, respectively. Thumbnail pictures depict representative species for each ecomorph: A. sagrei (trunk-ground), A. carolinensis (trunk-crown), A. luteogularis (crown-giant), A. occultus (twig), A. pulchellus (grass-bush), A. distichus (trunk). (B) Morphological variation was quantified on the basis of 18 3D landmarks on each of the pectoral and pelvic girdles (for more information, see Supplementary file 1A), the length of individual bones of both fore- and hindlimb, and bone thickness and bone cortical thickness of long bones. (A). thumbnail permissions: 'Image of A. sagrei (trunk-ground), courtesy of Brown, 2013, retrieved from https://commons.wikimedia.org/wiki/File:Cuban_Brown_Anole_(Anolis_sagrei)_(8592690316).jpg on 07/22/2020, distributed under the terms of the CC-BY 2.0 license.'.

© 2005 Daniel CD. Image of A. carolinensis (trunk-crown), courtesy of Daniel CD, 2005, retrieved from https://commons.wikimedia.org/wiki/File:Anole.jpg on 07/22/2020, distributed under the terms of the CC-BY-SA-3.0 license. It is not covered by the CC-BY 4.0 license and further reproduction of this panel would need to adhere to the terms of the CC-BY-SA-3.0 license.

© 2013 Allan Finlayson. Image of A. luteogularis (crown-giant), courtesy of Allan Finlayson, 2013, retrieved from https://www.inaturalist.org/photos/713126 on 07/22/2020, distributed under the terms of the CC-BY-NC 4.0 license. It is not covered by the CC-BY 4.0 license and further reproduction of this panel would need to adhere to the terms of the CC-BY-NC 4.0 license.

© 2016 Day's Edge Productions. Image of A. occultus (twig), reproduced with permission from Day's Edge Productions (c) 2016. It is not covered by the CC-BY 4.0 license and further reproduction of this panel would need permission from the copyright holder.

© 2011 Príncipe Castro. Image of A. pulchellus (grass-bush), courtesy of Príncipe Castro, 2011, retrieved from https://commons.wikimedia.org/wiki/File:Anolis_pulchellus_2.jpg on 07/22/2020, distributed under the terms of the CC-BY-SA 2.0 license. It is not covered by the CC-BY 4.0 license and further reproduction of this panel would need to adhere to the terms of the CC-BY-SA 2.0 license.

© 2011 Ianaré Sévi. Image of A. distichus (trunk), courtesy of Ianaré Sévi, 2011, retrieved from https://sv.wikipedia.org/wiki/Anolis_distichus#/media/Fil:Anolis_distichus_dewlap.jpg on 07/22/2020, distributed under the terms of the CC-BY-SA 3.0 license. It is not covered by the CC-BY 4.0 license and further reproduction of this panel would need to adhere to the terms of the CC-BY-SA 3.0 license.

Figure 2 with 1 supplement
Principal component analysis of 259 individual males from 95 Anolis species and their phylogenetic relationships.

(A) The first and second principal components on the level of individual explain 16.32% and 13.00% of the variance, respectively. The features that load most strongly on PC1 are the shape of the pelvic girdle and humerus length, and features loading strongly on PC2 are the shape of the pectoral girdle and bone cortical thickness (Supplementary file 1L). (B) Phylogenetic tree based on Poe et al., 2017 with the associated island of origin and ecomorph classification (Losos, 2009; Nicholson et al., 2012) per species. For more detailed results of species-level and phylogenetic principal component analysis, see Figure 2—figure supplement 1.

Figure 2—figure supplement 1
Principal component analysis of 259 individual males from 95 Anolis species in a phylogenetic context.

(A) The same principal component analyses as in the main Figure 2A, but using averages per species. (B) The same principal component plot as in panel A, but shown as a phylomorphospace. (C) The same principal component analyses as in panel A, but using averages per species and taking phylogeny into account (i.e., a ‘pPCA’; Revell, 2009). (D) The same phylogenetic component plot as in panel C, but shown as a phylomorphospace. Controlling for phylogenetic relationship reduces the clustering of ecomorphs (panels C and D), which reflects that each ecomorph evolved only a limited number of times, and that many members of an ecomorph class are closely related to each other. Grey dots in panels B and D are principal components of inferred ancestral species.

Schematic for assessing how well divergence between ecomorph pairs are aligned between islands.

The rationale of assessing the degree of alignment uses a vector-based approach in multivariate space, but is depicted for a schematic 2-trait space here to demonstrate the logic. The alignment of island pairs was quantified as the angle theta (Θ) between the two vectors that describe the trajectories between sets of two ecomorphs in multivariate space. An angle of zero implies that the two vectors are parallel. The same logic applies to the difference between the lengths (∆L) of the vectors. The trajectory between ecomorphs was calculated based on t-test statistics per trait (Adams and Collyer, 2009; see also Stuart et al., 2017). For thumbnail permissions, see Figure 1.

Figure 4 with 2 supplements
Alignment of the morphological difference between pairs of ecomorphs on the four Greater Antillean islands.

(A) A frequency plot of all 53 quartet comparisons (pairs of ecomorphs on island pairs) shows that all angles Θ are between 0° and 90° (mean: 54.44°; standard deviation: 12.57°). (B) A matrix of ecomorph pairs is used to visualize the significance level of parallelism between island pairs. Each line represents a pair of islands and the colour signifies if the angle is indistinguishable from 0° (red), significantly larger than 0°, but smaller than 90° (grey), or indistinguishable from 90° (blue). Significance levels were assessed using randomization and permutation tests (see Materials and methods).

Figure 4—figure supplement 1
Alignment of the morphological difference between pairs of ecomorphs on the four Greater Antillean islands separately for individual aspects of the locomotor apparatus.

Frequency plots of all 53 quartet comparisons (pairs of ecomorphs on island pairs) shows that the vast majority of angles Θ are between 0° and 90°. Frequency plots are shown for pectoral and pelvic girdles, limb length and bone thickness separately. The four plots are directly comparable to the plot in Figure 4A. Mean angles Θ are 57.97° (pectoral girdle), 53.19° (pelvic girdle), 54.57° (limb length) and 50.88° (bone thickness). Thus, the moderate degree of parallelism overall (Figure 4A) is consistent across individual aspects of the locomotor apparatus.

Figure 4—figure supplement 2
Rearing habitat used in locomotion-induced plasticity experiment.

Hatchlings of A. sagrei and A. carolinensis were raised in groups of six lizards in structurally different habitats, (A) ‘climbing’ habitat and (B) ‘running’ habitat. Animals were reared under these conditions until they reached 5 months of age, at which the majority of animals had reached sexual maturity (images show recently hatched lizards).

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