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The consequences of craniofacial integration for the adaptive radiations of Darwin’s finches and Hawaiian honeycreepers

Abstract

The diversifications of Darwin’s finches and Hawaiian honeycreepers are two text-book examples of adaptive radiation in birds. Why these two bird groups radiated while the remaining endemic birds in these two archipelagos exhibit relatively low diversity and disparity remains unexplained. Ecological factors have failed to provide a convincing answer to this phenomenon, and some intrinsic causes connected to craniofacial evolution have been hypothesized. The tight coevolution of the beak and the remainder of the skull in diurnal raptors and parrots suggests that integration may be the prevalent condition in landbirds (Inopinaves). This is in contrast with the archetypal relationship between beak shape and ecology in Darwin’s finches and Hawaiian honeycreepers, which suggests that the beak can adapt as a distinct module in these birds. Modularity has therefore been proposed to underpin the adaptive radiation of these groups, allowing the beak to evolve more rapidly and freely in response to ecological opportunity. Here, using geometric morphometrics and phylogenetic comparative methods in a broad sample of landbird skulls, we show that craniofacial evolution in Darwin’s finches and Hawaiian honeycreepers seems to be characterized by a tighter coevolution of the beak and the rest of the skull (cranial integration) than in most landbird lineages, with rapid and extreme morphological evolution of both skull regions along constrained directions of phenotypic space. These patterns are unique among landbirds, including other sympatric island radiations, and therefore counter previous hypotheses by showing that tighter cranial integration, not only modularity, can facilitate evolution along adaptive directions.

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Fig. 1: How integration and selection direct phenotypic evolution.
Fig. 2: Pattern and tempo of craniofacial evolution in landbirds.
Fig. 3: Evolutionary integration between the beak and the skull in landbirds.
Fig. 4: Strength of cranial integration across landbirds and maximum phenotypic distance in each family or subfamily.

Data availability

All relevant data are available via the University of Bristol’s DataBris repository at https://data.bris.ac.uk/data/dataset/3kpwgpnqewcy2tvak6uzzdztt.

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Acknowledgements

We thank J. Cooper and J. White (NHM Tring), and C. M. Milensky and B. K. Schmidt (Smithsonian National Museum of Natural History) for access to specimens. We thank F. Blanco, M. Fabbri, I. Menéndez and L. Porras for discussions on the evolutionary implications of this research. We thank G. Thomas, T. Püschel, C. Klingenberg, A. Elsler, F. Babarović and S. de Esteban-Trivigno for insight and discussion on the methods. We thank Ó. Sanisidro and L. Balsa Pascual for design and technical advice that greatly improved the quality of the graphic support. G.N. was supported by a PG Scholarship/Studentship from the Alumni Foundation, University of Bristol, UK, and is currently supported by the ERC project ‘TEMPO’ (grant number 639791). J.M.-L. is supported by the Spanish MINECO, Project CGL-2013-42643. E.J.R. and J.A.B. were supported by BBSRC grant number BB/I011668/1. C.R.C. is supported by a Leverhulme Early Career Fellowship (grant number ECF-2018-101).

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The focus and design of this research were developed by G.N., J.M.-L., J.A.B. and E.R.J. C.R.C. conducted the VRMAs. G.N. conducted the remaining analyses. G.N., J.M.-L., J.A.B., C.R.C. and E.R.J. wrote the manuscript.

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Correspondence to Guillermo Navalón or Emily J. Rayfield.

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Extended data

Extended Data Fig. 1 Landmarks and semilandmarks used in this study for the beak (white) and skull (black) blocks.

Landmark definition in Extended Data Table 1.

Extended Data Fig. 2

Landmarks used in this study. **Cracraft, J. The lacrimal-ectethmoid bone complex in birds: a single character analysis. American Midland Naturalist, 316-359 (1969).

Extended Data Fig. 3 Tempo and mode of craniofacial shape evolution in landbirds (labelled by major radiations).

Phylomorphospaces of the first three PCs (a) and rates of evolution (b) for the whole skull configurations. Dot colours in phylomorphospaces (a) correspond to each major 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 Data Fig. 4 Tempo and mode of beak shape evolution in landbirds (labelled by major radiations).

Phylomorphospaces of the first three PCs (a) and rates of evolution (b) for the beak block configurations. Colours and legends as before.

Extended Data Fig. 5 Tempo and mode of skull shape evolution in landbirds (labelled by major radiations).

Phylomorphospaces of the first three PCs (a) and rates of evolution (b) for the skull block configurations. Colours and legends as before.

Extended Data Fig. 6 Shape differences associated with the first pair of PLS vectors (PLS1) for the beak block and the skull block for the main lineages of passerines.

Polar histograms summarizing angle comparisons between the PLS1 vectors for the beak (b) and skull (c) blocks. As orientation of PLS1 vectors is arbitrary, the maximum possible angle between PLS1 vectors is 90°. * indicates single angular comparison of the PLS1 vectors of Passeroidea excluding DF and HH.

Extended Data Fig. 7 Extreme morphologies and spread along lines of least resistance for each family within the parvorder Passeroidea in our sample.

Within-family maximum Procrustes distances for PLS1scores (situation 2) for both beak and skull blocks. Done for all the families that include two or more species in our sample. Legend for labels in Extended Data Table 2. Dot colours correspond to the ages of the most common recent ancestor (MRCA) for each of the focal families in our MCC tree.

Extended Data Fig. 8 Relationship between levels of cranial integration and evolutionary rates per clade.

Dotplot showing the relationship between mean and median log-rate per landbird/passerine clade (clades as defined in Figs. 3, 4 and Table 1) with mean clade zscore values (that is 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 Data Fig. 9 Legend for family names.

Fig. 4c, d and Extended Data Figure 6.

Extended Data Fig. 10 Comparisons of the pattern of maximum covariation lines between Passeroidea and other selected passerine clades.

Angles (θ, degrees) for each pair of PLS1 vectors for the beak and skull block in situation 2 between Passeroidea (including and excluding DF and HH), Muscicapida (the parvorder that includes the passerine radiations sympatric to DF 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.

Supplementary information

Supplementary Information

Extended results, Supplementary Figs. 1–6, Tables 1–3 and references.

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Supplementary Data Tables 1–5.

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Navalón, G., Marugán-Lobón, J., Bright, J.A. et al. The consequences of craniofacial integration for the adaptive radiations of Darwin’s finches and Hawaiian honeycreepers. Nat Ecol Evol 4, 270–278 (2020). https://doi.org/10.1038/s41559-019-1092-y

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