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The Consequences of Craniofacial Integration for the Adaptive Radiations of Darwin’S Finches and Hawaiian Honeycreepers

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The Consequences of Craniofacial Integration for the Adaptive Radiations of Darwin’S Finches and Hawaiian Honeycreepers This is a repository copy of The consequences of craniofacial integration for the adaptive radiations of Darwin’s finches and Hawaiian honeycreepers. White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/157037/ Version: Accepted Version Article: Navalón, G., Marugán-Lobón, J., Bright, J.A. et al. (2 more authors) (2020) The consequences of craniofacial integration for the adaptive radiations of Darwin’s finches and Hawaiian honeycreepers. Nature Ecology & Evolution, 4 (2). pp. 270-278. https://doi.org/10.1038/s41559-019-1092-y This is a post-peer-review, pre-copyedit version of an article published in Nature Ecology and Evolution. 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[email protected] https://eprints.whiterose.ac.uk/ Figure # Figure title Filename Figure Legend One sentence only This should be the If you are citing a reference for the first time name the file is saved in these legends, please include all new as when it is uploaded references in the Online Methods References to our system. Please section, and carry on the numbering from the include the file main References section of the paper. extension. i.e.: Smith_ED Fig1.jpg Extended Extended Data Figure EXTENDED DATA Landmark definition in Extended Data Fig. 1 | Landmarks and FIGURE 1.tif Data Table 1. 1 semilandmarks used in this study for the beak (white) and skull (black) blocks. Extended Extended Data Figure EXTENDED DATA Data Fig. 2. Landmarks used in FIGURE 2. 2 this study. LANDMARK DEFINITION.tif Extended Extended Data Figure EXTENDED DATA Phylomorphospaces of the first three Data Fig. 3 | Tempo and mode of FIGURE 3.tif PCs (A) and rates of evolution (B) 3 craniofacial shape for the whole skull configurations. evolution in landbirds Dot colours in phylomorphospaces (labelled by major (A) correspond to each major radiations). landbird lineage (colour legend by each silhouette in B). Branch colours in B indicate relative rate of shape evolution. Inferred rate shifts with higher posterior probability than 0.7 are plotted in corresponding branches (circles) or nodes (triangles) in the phylogeny in B. Posterior probability of each inferred rate shift is indicated by size as indicated in the legend in B. Extended Extended Data Figure EXTENDED DATA Phylomorphospaces of the first three Data Fig. 4 | Tempo and mode of FIGURE 4.tif PCs (A) and rates of evolution (B) 4 beak shape evolution for the beak block configurations. in landbirds (labelled Colours and legends as before. by major radiations). Extended Extended Data Figure EXTENDED DATA Phylomorphospaces of the first three Data Fig. 5 | Tempo and mode of FIGURE 5.tif PCs (A) and rates of evolution (B) skull shape evolution for the skull block configurations. 5 in landbirds (labelled Colours and legends as before. by major radiations). Extended Extended Data Figure EXTENDED DATA Polar histograms summarizing angle Data Fig. 6 | Shape differences FIGURE 6.tif comparisons between the PLS1 6 associated with the vectors for the beak (B) and skull first pair of PLS (C) blocks. As orientation of PLS1 vectors (PLS1) for the vectors is arbitrary, the maximum beak block and the possible angle between PLS1 skull block for the vectors is 90°. * indicates single main lineages of angular comparison of the PLS1 passerines. vectors of Passeroidea excluding DF and HH. Extended Extended Data Figure EXTENDED DATA Within-family maximum Procrustes Data Fig. 7 | Extreme FIGURE 7.tif distances for PLS1scores (situation 7 morphologies and 2) for both beak and skull blocks. spread along lines of Done for all the families that include least resistance for two or more species in our sample. each family within the Legend for labels in Extended Data parvorder Passeroidea Table 2. Dot colours correspond to in our sample. the ages of the most common recent ancestor (MRCA) for each of the focal families in our MCC tree. Extended Extended Data Figure EXTENDED DATA Dotplot showing the relationship Data Fig. 8 | Relationship FIGURE 8.tif between mean and median log-rate 8 between levels of per landbird/passerine clade (clades cranial integration and as defined in Figures 3, 4 and Table evolutionary rates per 1) with mean clade zscore values clade. (i.e. evolutionary covariation, situation 2). Dashed ellipses encompass the values for selected clades: 1, All landbirds; 2, Non- passerines; 3, Passeriformes; 4, Passeri; 5, Tyranni; 6, Psittaciformes; P.1, Passeroidea (including Darwin’s finches and Hawaiian honeycreepers); P.2. Passeroidea (excluding Darwin’s finches and Hawaiian honeycreepers). Extended Extended Data Figure EXTENDED DATA Figure 4c, 4d and Extended Data Data Fig. 9 | Legend for family FIGURE 9.tif Figure 6. 9 names. Extended Extended Data Figure EXTENDED FIGURE Angles (, degrees) for each pair of Data Fig. 10 | Comparisons of 10.tif PLS1 vectors for the beak and skull 10 the pattern of block in situation 2 between maximum covariation Passeroidea (including and lines between excluding DF and HH), Muscicapida Passeroidea and other (the parvorder that includes the selected passerine passerine radiations sympatric to DF clades. and HH) and Passeriformes, Passeri (all oscine passerines) and Tyranni (all suboscine passerines). As orientation of PLS1 vectors is arbitrary, the maximum possible angle between PLS1 vectors is 90°. * excluding DF and HH. 1 Item Present? Filename A brief, numerical description of file This should be the name the file is saved as when it is contents. uploaded to our system, and should include the file extension. The extension must be .pdf i.e.: Supplementary Figures 1-4, Supplementary Discussion, and Supplementary Tables 1-4. Supplementary Yes SI_FINAL_TEXT.pdf Extended Results, Information Supplementary Figures 1-6, Supplementary Table 1-3, Supplementary References Reporting Yes Navalon_et_al_reporting_summary.pdf Summary 2 3 Number Filename Type Legend or If there are multiple files This should be the name the file is saved as Descriptive of the same type this when it is uploaded to our system, and should Caption should be the numerical include the file extension. i.e.: Smith_ indicator. i.e. “1” for Video Supplementary Video 1.mov Describe the 1, “2” for Video 2, etc. contents of the file Supplementary Supplementary Data Supplementary Data SUPPLEMENTARY_DATA_ALL.xlsx Data Tables 1-5 4 5 Title: The consequences of craniofacial integration on the adaptive 6 radiations of Darwin’s Finches and Hawaiian Honeycreepers 7 Guillermo Navalón1,2,3*, Jesús Marugán-Lobón2,4, Jen A. Bright5,6, Christopher R. Cooney7 & 8 Emily J. Rayfield1,* 9 1. School of Earth Sciences, University of Bristol, Life Sciences Building, Bristol, UK 10 2. Unidad de Paleontología, Departamento de Biología, Universidad Autónoma de Madrid, Madrid, Spain 11 3. Department of Earth Sciences, University of Oxford, Oxford OX1 3AN, United Kingdom. 12 4. Dinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles, CA, USA. 13 5. School of Geosciences, University of South Florida, Tampa, FL 33620, USA 14 6. Department of Biological and Marine Sciences, University of Hull, Hull HU6 7RX, UK7.Department of Animal and Plant 15 Sciences, University of Sheffield, Sheffield S10 2TN, UK. 16 *Corresponding authors. E-mails: [email protected], [email protected] 17 18 The diversification of Darwin’s finches and Hawaiian honeycreepers are two textbook 19 examples of adaptive radiation in birds. Why these two bird groups radiated while the 20 remaining endemic birds in these two archipelagos exhibit relatively low diversity and 21 disparity remains unexplained. Ecological factors have failed to provide a convincing 22 answer to this phenomenon, and some intrinsic causes connected to craniofacial 23 evolution have been hypothesized. Tight coevolution of the beak and the remainder of 24 the skull in diurnal raptors and parrots suggests that integration may be the prevalent 25 condition in landbirds (Inopinaves). This is in contrast with the archetypal relationship 26 between beak shape and ecology in Darwin’s finches and Hawaiian honeycreepers, 27 which suggests the beak can adapt as a distinct module in these birds. Modularity has 28 therefore been proposed to underpin the adaptive radiation of these birds, allowing the 29 beak to evolve more rapidly and ‘freely’ in response to ecological opportunity. Here, 30 using geometric morphometrics and phylogenetic comparative methods in a broad 31 sample of skulls of landbirds, we show that craniofacial evolution in Darwin’s finches 32 and Hawaiian honeycreepers appears to be characterized by a tighter coevolution of the 33 beak and the rest of the skull (cranial integration) than in most landbird lineages, with 34 rapid and extreme morphological evolution of both skull regions along constrained 35 directions of phenotypic space. These patterns are unique among landbirds, including 36 other sympatric island radiations, and therefore counter previous hypotheses by 37 showing that tighter cranial integration, not only modularity, can facilitate evolution 38 along adaptive directions. 39 Why some lineages diversify more or less than others is a central topic in evolutionary 40 biology. Among birds, the adaptive island radiations of Darwin’s finches and Hawaiian 41 honeycreepers are notable for their rapid and disparate evolution1,2.
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