Abstract
An important question in the study of phenotypic evolution is whether characters are independent of each other or behave and evolve as integrated modules. Morphological integration and modularity provide a powerful framework for the analysis of the evolution of morphological traits. We used geometric morphometrics and phylogenetically independent contrasts (PIC) to test four different modularity hypotheses in the haptoral anchors of 14 monogenean species of Ligophorus. Integration between the modular units identified was further evaluated with two-block partial least squares analysis. Roots and points represented two modules in the dorsal and ventral anchors, but modularity was not statistically supported when parasite phylogeny was accounted for, which may indicate convergent evolution related to host characteristics and gill morphology. In contrast, PIC revealed medial and lateral modules in ventral anchors only. Moreover, we found evidence for ventral and dorsal anchor pairs forming two modules, supporting the notion that they play different functional roles. Integration between all identified modules was strong. We conclude that there is modular structure in the anchors of Ligophorus spp., accounted by adaptive and phylogenetic factors acting at different levels, and ventral and dorsal anchors evolve as integrated modules with specific roles in attachment.
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Acknowledgments
A.R.G. benefited from a PhD student grant from the Consejo Nacional de Ciencia y Tecnología (CONACyT-CONCYTEY) of the Mexican Government and Yucatan State, Mexico (scholarship no. 204397), National Plan for Scientific Research, Development and Technological Innovation of Spain (CGL2008-02701), the Generalitat Valenciana, Spain (Prometeo Project 2015/018), and Ministry of Economy and Competitivity, Spain (CGL2015-71146).
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Fig. S1
Phylogenetic tree of Ligophrous spp. from the Mediterranean and Black Sea derived from Bayesian inference and maximum likelihood analysis using the 28S and ITS1 regions. Posterior probability values are indicated above the branches, followed by maximum likelihood bootstrap values (in %). Posterior probabilities <0.80 and bootstrap values <60 % not reported (GIF 17 kb)
Fig. S2
Analysis of modularity in the ventral and dorsal anchors. Graphs show the RV coefficients for the subdivision of landmarks into anchors and the distribution of RV coefficients, for 10,000 alternative partitions of landmarks into anatomically contiguous (H1 and H3) and non-contiguous (H2) subsets (histograms). A–C represents ventral anchors, and D–F represents dorsal anchors. Black arrows indicate the observed RV coefficients value and black stars indicate significant partitions (GIF 39 kb)
Fig. S3
Analysis of modularity in the ventral–dorsal anchors (H4). Graphs show the RV coefficients for the subdivision of landmarks in separate anchors and the distribution of RV coefficients, for 10,000 alternative partitions of landmarks in anatomically non-contiguous subsets (histogram). Black arrows indicate the observed RV coefficients value and black stars indicate significant partitions (GIF 13 kb)
Fig. S4
Evolutionary analysis of modularity in ventral and dorsal anchors with Phylogenetic independent contrasts (PIC). Graphs show the RV coefficients for the subdivision of landmarks into anchors and the distribution of RV coefficients, for 10,000 alternative partitions of landmarks into anatomically contiguous H1 and H3 and non-contiguous H2. A–C represents ventral anchors, and D–F represents dorsal anchors. Black arrows indicate the observed RV coefficients value and black stars indicate significant partitions (GIF 40 kb)
Fig. S5
Evolutionary analysis of modularity in the ventral–dorsal anchors (H4). Graphs show the RV coefficients for the subdivision of landmarks in separate anchors and the distribution of RV coefficients, for 10,000 alternative partitions of landmarks in anatomically non-contiguous subsets (histogram). Black arrows indicate the observed RV coefficients value and black stars indicate significant partitions (GIF 13 kb)
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Rodríguez-González, A., Míguez-Lozano, R., Sarabeev, V. et al. Evolutionary modularity and morphological integration in the haptoral anchor structures of Ligophorus spp. (Monogenea: Dactylogyridae). Parasitol Res 115, 3519–3533 (2016). https://doi.org/10.1007/s00436-016-5117-z
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DOI: https://doi.org/10.1007/s00436-016-5117-z