DOI: 10.5061/dryad.4tmpg4fmv
title: Craniofacial modularity and cranial kinesis evolution in the adaptive radiation of Furnariidae (Aves: Passeriformes)

description: The role of phenotypic modularity in the evolution of skull morphology in
 birds has been a subject of debate in recent years. Furnariids (ovenbirds,
 woodcreepers, and allies), a spectacular avian adaptive radiation, are
 distinguished in their cranial morphology as the only passerines with two
 types of cranial kinesis, constituting a great model to test whether the
 evolution of novelties in cranial kinesis was associated with shifts in
 patterns of evolutionary modularity and allometry in the avian skull. Our
 analyses by means of geometric morphometric tools and phylogenetic
 comparative methods show that the beak and neurocranium of furnariids
 evolved in a modular fashion and were shaped by the cranial kinesis
 evolution. Besides, species with prokinesis show a higher degree of
 modularity and morphological disparity, lower phenotypic rates, as well a
 higher contribution of allometry in the evolution of the beak morphology
 than species with proximal rhynchokinesis, suggesting, as observed in
 several vertebrates, that the functional demands associated with higher
 degrees of cranial kinesis promoted rapid integration throughout the
 skull. Prokinetic - robust morphotypes and proximal rhynchokinetic -
 gracile morphotypes, have repeatedly evolved by evolutionary convergence
 in both evolutionary modules, which suggests the existence of functional
 trade-offs and long-standing adaptive optima related to cranial kinesis.
description: Data sampling  
 Skull morphology was studied on photographs taken in lateral and
 dorsal view of 153 museum skeleton specimens representing 106 species, 51
 genera (covering 73% of all currently recognized genera; sensu Clements et
 al., 2022), three subfamilies (i.e., Sclerurinae, Dendrocolaptinae, and
 Furnariinae), and all monophyletic clades of Furnariidae (i.e., tribes;
 sensu Harvey et al., 2020) (see Supplementary Table S1 for information on
 each specimen examined in this study). Although subtle differences in size
 between males and females have been reported in some traits in certain
 species of furnariids (e.g., Moreno et al., 2007; Diniz et al., 2016),
 there is no significant sexual dimorphism reported in the skulls of these
 birds (Stefanini et al., 2016). Therefore, our sampling did not
 discriminate between sexes.  Morphological
 quantification  Variation in
 skull shape was quantified in 110 specimens representing 83 species (see
 Supplementary Table S1) using 17 landmarks and 30 curve semilandmarks,
 digitized on photographs taken in lateral view of each specimen using
 Stereomorph (v. 1.6.7) (Olsen & Westneat, 2015) (Figure 2;
 Supplementary Figure S1A). Landmarks were mainly taken from Marugán-Lobón
 & Buscalioni (2006) and Navalón et al. (2020) (see description of
 each landmark in Table 1). Since we were particularly interested in
 capturing the variation associated with the cranial kinesis, we added one
 landmark to quantify the presence and extension of the rhynchokinetic
 'slit-like gap' hinge (hinge E in Zusi, 1984), which is formed
 in the junction between the lateral and ventral bar (see Figure 1A, B).
 Moreover, we quantified the contour of the external naris fossa in order
 to reflect the variation of pseudo-schizorhinal and holorhinal nares
 linked to proximal rhynchokinesis and prokinesis respectively (Figure 1).
 In the neurocranium, traits that were related to the pterygoid and
 quadrate bones were quantified, since these elements belong to the
 osteological complex involved in cranial kinesis (Bock, 1964). In
 addition, traits linked to the degree of ossification, such as those
 related to the fenestrae of the interorbital septum as well as the traits
 related to the temporal fossa and zygomatic process were quantified to
 capture the variation associated with the gracile and robust morphotypes
 which are frequently linked to proximal rhynchokinesis and prokinesis,
 respectively (Figure 1A).  To
 avoid introducing unnatural variation (i.e., artifacts of preservation;
 Adams, 1999; Rhoda et al. 2021b) due to the disarticulation of elements,
 such as those involved in the multi-bar linkage system (e.g., jugal bar,
 quadrate, pterygoid, palatal elements, and beak), we only included species
 represented by complete dry skulls that had no signs of deformation in the
 geometric morphometric analyses. In passerine bird skulls, this ensures
 that the angles between the different anatomical regions remain
 constant.  Curve semilandmarks
 (Bookstein, 1997) capturing the shape of the naris, tomium, and culmen
 were slid until minimizing the bending energy (Gunz et al., 2005).
 Differences in scale, position, and orientation among specimens were
 removed by means of Generalized Procrustes Analysis (hereafter GPA, Gower,
 1975). Total skull size was measured using the log-transformed centroid
 size (log-Cs) of each specimen prior to GPA.  
 To obtain species means of shapes and sizes,
 Procrustes shape coordinates and log-Cs were averaged within each species.
 The mean Procrustes coordinates retrieved were subjected to a new round of
 GPA superimposition to obtain the shape coordinates that include
 allometric variation (hereafter full-shape). In addition, a second set of
 shape coordinates devoid of allometric variation (hereafter non-allometric
 shape) was estimated by computing the phylogenetically corrected shape
 residuals resulting from the linear regression of the full-shape on log-Cs
 (Klingenberg, 1996; Revell, 2009). To obtain summarized information on the
 variation of shape that would allow, on the one hand, an exploratory
 assessment of the data and, on the other hand, the assessment of the
 evolutionary convergence and the rates of phenotypic evolution, a
 principal component analysis (PCA) was carried out for the entire skull
 and on the neurocranium and beak (i.e., rostrum including naris) for both
 datasets (i.e., full-shape and non-allometric shape). 
 For the sake of brevity, the description
 of full-shape variation summarized by the meaningful Principal Components
 (PCs) of the neurocranium and the beak (i.e., those PCs retained with the
 Broken Stick method; Jackson, 1993) are provided in Appendix S1 of
 Supplementary Information. With the aim of graphically representing the
 variation associated with common ancestry, the morphospaces generated by
 the first two principal components of the entire skull, neurocranium, and
 beak for full-shape and non-allometric shape (Figure 3A and Figure 4A, B,
 C, D; see also Supplementary Figure S2A, B for morphospaces with tips
 labelled with species names) were depicted following a phylomorphospace
 approach (Sidlauskas, 2008). All the analyses were performed within the R
 programming environment (R Core Team, 2022) using the Morpho (v. 2.12)
 (Schlager, 2017), geomorph (v. 4.0.8) (Baken et al. 2021, Adams et al.,
 2023), morphospace (v. 0.009) (Milla Carmona, 2022), and phytools (v.
 2.3-0) (Revell, 2012) packages.
description: # Craniofacial modularity and cranial kinesis evolution in the adaptive
 radiation of Furnariidae (Aves: Passeriformes)
 [https://doi.org/10.5061/dryad.4tmpg4fmv](https://doi.org/10.5061/dryad.4tmpg4fmv) ### Files and variables #### File: Furnariidae\_cranial\_kinesis\_Variables.csv **Description:** Variables associated with cranial kinesis used in phylogenetic comparative methods. * Species: Species used in geometric morphometric analyses and PCM * Kinesis: A binary variable derived from the discretization of the range of values adopted by the kinetic index. * Indice_Kinetico: A variable constructed from the sum of the states of three variables associated with cranial kinesis. #### File: Phylogenetic\_trees.zip **Description:** The complete phylogenetic tree obtained by Harvey et al. (2020) and the three pruned variations used in the present study. #### File: Neurocranium.zip **Description:** Landmark coordinates obtained with Stereomorph of all specimens per species. Neurocranium Procrustes coordinates and Centroid Size: a proxy for size (Centroid Size) and Procrustes coordinates with and without allometric variation of species means as used in the PCM. #### File: Skull\_Prokinetic\_sps.zip \**Description: **Landmark and sliding semilandmarks coordinates obtained with Stereomorph of all specimens per prokinetic species (45sps). Skull Procrustes coordinates and Centroid Size: a proxy for size (Centroid Size) and Procrustes coordinates with and without allometric variation of species means as used in the PCM.  #### File: Skull\_Proximal\_rhynchokinetic\_sps.zip **Description:** Landmark and sliding semilandmarks coordinates obtained with Stereomorph of all specimens per proximal rhynchokinetic species (38sps). Skull Procrustes coordinates and Centroid Size: a proxy for size (Centroid Size) and Procrustes coordinates with and without allometric variation of species means as used in the PCM.  #### File: Skull.zip **Description:**  Landmark and sliding semilandmarks coordinates obtained with Stereomorph of all specimens per species (83 sps). Skull Procrustes coordinates and Centroid Size: a proxy for size (Centroid Size) and Procrustes coordinates with and without allometric variation of species means as used in the PCM.  #### File: Beak.zip **Description:**  Landmark and sliding semilandmarks coordinates obtained with Stereomorph of all specimens per species (83 sps). Beak Procrustes coordinates and Centroid Size: a proxy for size (Centroid Size) and Procrustes coordinates with and without allometric variation of species means as used in the PCM.  ## Code/software Free available R packages: Stereomorph, geomorph, ape, phytools, magrittr, morphospace, mvMORPH, Morpho, RRphylo ## Access information NA