Rapid diversification associated with a macroevolutionary pulse of developmental plasticity

  1. Vladislav Susoy
  2. Erik J Ragsdale  Is a corresponding author
  3. Natsumi Kanzaki
  4. Ralf J Sommer  Is a corresponding author
  1. Max Planck Institute for Developmental Biology, Germany
  2. Indiana University, United States
  3. Forestry and Forest Products Research Institute, Japan
4 figures, 1 table and 1 additional file

Figures

Mouth dimorphism and novelty in Diplogastridae.

(A) The diplogastrid eurystomatous (Eu) morph, as shown here for Parapristionchus giblindavisi, is marked by a wider mouth, larger teeth, and often greater stomatal complexity than the …

https://doi.org/10.7554/eLife.05463.003
A radiation of feeding structures in diplogastrid nematodes.

(A) Phylogenetic relationships inferred for nematodes of Rhabditina, including 54 species of Diplogastridae (Figure 2—source data 1A,B) from an alignment including SSU rRNA, LSU rRNA, and 11 …

https://doi.org/10.7554/eLife.05463.006
Figure 2—source data 1

Nematode taxa used in this study, with isolation details given.

(A) Origins of strains are coded as follows: CGC, Caenorhabditis Genetics Center; JB, Baldwin lab (U. California, Riverside); MV, Viney lab (U. Bristol); NK, Kanzaki lab; RGD, Giblin-Davis lab (U. Florida-IFAS); RS, Sommer lab; SB, Sudhaus lab (Freie Universität Berlin). For other strains, references are given. nc, not culturable. (B) GenBank accession numbers for gene sequences analyzed in this study. Sequences shorter than 200 bp (with accession numbers beginning with ‘VS’) are available at www.pristionchus.org/download/suppSusoy2014.html.

https://doi.org/10.7554/eLife.05463.007
Figure 3 with 3 supplements
Developmental plasticity, morphological disparity, and evolutionary tempo in diplogastrid nematodes.

(A) Stomatal morphology and positions of 11 two-dimensional landmarks (taxa coded in Figure 2). Below is a projection of the first two principal components of stomatal shape-space. Purple circles …

https://doi.org/10.7554/eLife.05463.008
Figure 3—source data 1

Results from analyses of principle components, disparity, and evolutionary rates.

(A) Results of principal component analysis of stomatal form in Rhabditina, including both morphs of dimorphic taxa.

Loadings of Procrustes coordinates and log centroid size of stomatal form onto the first four principal component (PC) axes are shown, as are the proportion of variance explained by those PC axes (B) Results of principal component analysis of stomatal shape in Rhabditina, including both morphs of dimorphic taxa. Loadings of Procrustes coordinates of stomatal shape onto the first four principal component (PC) axes are shown, as are the proportion of variance explained by those PC axes. (C) Results of phylogenetic principal component analysis of stomatal form in Rhabditina, with dimorphic taxa represented by the stenostomatous (St) morph. Loadings of Procrustes coordinates and log centroid size of stomatal form onto the first four principal component (PC) axes are shown, as are the proportion of variance explained by those PC axes. (D) Results of phylogenetic principal component analysis of stomatal shape in Rhabditina, with dimorphic taxa represented by the stenostomatous (St) morph. Loadings of Procrustes coordinates of stomatal shape onto the first four principal component (PC) axes are shown, as are the proportion of variance explained by those PC axes. (E) Estimates of morphological disparity of the stoma in Rhabditina. Groups compared were non-diplogastrid Rhabditina, monomorphic Diplogastridae, and dimorphic Diplogastridae. Disparity was measured as the principal component (PC) analysis volume and the sum of univariate variances. PC scores along the first two and three PC axes of Procrustes form and shape space, respectively, were used and are presented in the form mean ± standard deviation (95% confidence interval). Eu, eurystomatous; St, stenostomatous. (F) Rates of stomatal evolution along the first principal component (PC) axis of Procrustes form- and shape-space. Rates were compared for non-diplogastrid Rhabditina (Rh), dimorphic Diplogastridae (Dm), and monomorphic Diplogastridae (Mn). Numbers indicate separate rate parameters for the designated groups. Model-averaged rates with standard deviation are shown. (G) Statistical comparison of non-nested models of stomatal evolution along the first principal component (PC) axis of Procrustes form- and shape-space using a chi-square distribution. Numbers indicate separate rate parameters for the designated groups. Rh, non-diplogastrid Rhabditina (Rh); Dm, dimorphic Diplogastridae; Mn, monomorphic Diplogastridae. (H) Highest posterior densities (HPD) of rates, and associated p-values obtained from two-tailed randomization tests, of stomatal form and shape evolution. Tests were performed for the branches assigned to non-diplogastrid Rhabditina, dimorphic Diplogastridae, and monomorphic Diplogastridae. CI, confidence interval.

https://doi.org/10.7554/eLife.05463.009
Figure 3—figure supplement 1
Projections of the first two principal components of Procrustes morphospace of stomatal landmarks.

In phylogenetic principal components analysis (phylogenetic PCA), dimorphic species are represented by the St morph. Purple circles represent non-diplogastrid Rhabditina (Rh), green circles mark …

https://doi.org/10.7554/eLife.05463.010
Figure 3—figure supplement 2
Rate estimates of stomatal shape evolution in Rhabditina.

In dimorphic taxa, rates are for St morph. Branch color indicates rates of evolutionary change; posterior rates are color-coded in legend.

https://doi.org/10.7554/eLife.05463.011
Figure 3—figure supplement 3
Posterior densities of rates of stomatal form and shape evolution in Rhabditina.

Bars below represent highest posterior density intervals of weighted rate estimates for the groups. Rh, non-diplogastrid Rhabditina; Dm, dimorphic Diplogastridae; Mn, monomorphic Diplogastridae. (A) …

https://doi.org/10.7554/eLife.05463.012
Figure 4 with 1 supplement
Correlation of polyphenism and complexity of nematode mouthparts.

Painted branches show congruence of simulated character histories of dimorphism (right tree; 0 = absent, 1 = present) and stomatal complexity (left tree; complexity index ranges from 0 to 9). …

https://doi.org/10.7554/eLife.05463.013
Figure 4—source data 1

Matrix of structures tabulated to measure stomatal complexity.

Structures were recorded as described in text. Presence/absence of dimorphism is also given. 0 = absence, 1 = presence.

https://doi.org/10.7554/eLife.05463.014
Figure 4—figure supplement 1
Tabulating complexity of nematode mouthparts.

The complexity index (ci) was tabulated as the sum of all stomatal ‘structures’, that is, geometric deviations marked by a <135° vertex from the cylindrical walls of the stoma or from the arched …

https://doi.org/10.7554/eLife.05463.015

Tables

Table 1

Environmental regulation of the mouth dimorphism across diplogastridae

https://doi.org/10.7554/eLife.05463.004
Dimorphic nematode speciesTreatment type% Eu, treatment% Eu, controlOdds ratio
Allodiplogaster sp. 1Prey1000
Allodiplogaster sudhausiPrey9711080.976
Diplogasteriana n. sp.Starved240
Fictor stercorariusPrey960
Koerneria luziaeStarved50
Micoletzkya inediaPrey950
Micoletzkya japonicaPrey920
Mononchoides sp. 1Prey9810120.272
Mononchoides sp. 3Prey1006
Neodiplogaster sp.Prey1000
Parapristionchus giblindavisiStarved3468.428
  1. The presence of prey nematode (C. elegans) larvae and the absence of bacterial food (‘prey’ treatment) induced development of the Eu morph in strains normally St-biased on an abundance of bacterial food (control). For species that could not reach adulthood on this regimen, conditions of overpopulation and starvation (‘starved’ treatment) similarly promoted the Eu morph. Effect size is given as the odds ratio (Fisher's exact test) where not infinite.

Table 1—source data 1

Environmental induction of the Eu morph in dimorphic species. Results for individual replicates (plates) are shown.

https://doi.org/10.7554/eLife.05463.005

Additional files

Supplementary file 1

Two tree files and a multiple sequence alignment file.

https://doi.org/10.7554/eLife.05463.016

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