MORPHOLOGICAL VARIATION IN THE AVIAN PELVIS by Rachel A. Frigot A thesis submitted to Johns Hopkins University in conformity with the requirements for the degree of Master of Science Baltimore, Maryland June 2019 © 2019 Rachel Frigot All rights reserved Abstract The hind-limb and its associated girdle perform a number of important functions in birds, including locomotion, feeding and reproduction. This has given rise to a number of efforts to correlate morphology of the hind-limbs to function, both to better understand the anatomy of living birds, and to infer the ecology of extinct ones. However, most of these studies have focused on the long bones of the hind-limb or have only considered narrow functional groups. This thesis examines the pelvis of forty-two species of birds using three-dimensional geometric morphometrics, examining the morphology of six different hind-limb functional groups. Morphology is tested against body size and phylogenetic frameworks. A poor correlation is found between body size and morphology when Procrustes variables are regressed against species mass and against centroid size. Differences in morphology are found between functional groups, and pair-wise comparisons suggest that the pelvic morphology of carnivores is significantly different from all other functional groups, and that divers are significantly different from all other groups except paddlers. These relationships do not become less significant when phylogeny is taken into account and projecting phylogeny into shape space demonstrates extensive lability of pelvic morphology, suggesting that function has a greater influence over morphology than phylogeny. A brief exploration of sexual dimorphism shows that any shape differences between male and female individuals are, at best, a small contribution to total shape variation, and hint that sexually dimorphic shape changes might be restricted to smaller clades within birds. This agrees broadly with the morphological literature on bird ii hind-limb morphology, and supports the use of morphology when making functional inferences about the hind-limb of extinct taxa. Primary Reader: Adam D. Sylvester Secondary Reader: Christopher Ruff iii Contents Abstract . ii List of Tables . v List of Figures . vi Introduction . 1 Materials and Methods . 8 Results . 19 Conclusions and discussion . 29 References . 41 Appendix 1 . 63 Curriculum Vitae . 70 iv List of Tables Table 1: Details of taxa used for the analysis . .10-11 Table 2 – Definitions of landmarks and curves defined by landmarks . 15 Table 3: MANOVA results of principal component scores, using hind-limb functional group as a factor . 28 Table 4: Results of pairwise Hotelling’s T2 test between functional hindlimb groups . 28 v List of Figures Figure 1: Placement of landmarks . 14 Figure 2: Scaled phylogenetic tree modified from Prum et al. (2015) . 18 Figure 3: Results of principal components analysis (PCA) . 21 Figure 4: Maximum and minimum scoring shape configurations for each of the first six principal components . 22 Figure 5: Plots of shape (Procrustes regression score) against size . 23 Figure 6: Box plots of between-group principal component scores for male and female specimens . 24 Figure 7: Plot of PC1 against PC2 for all specimens, with specimens coloured according to sex . 24 Figure 8: Phylomorphospace showing phylogeny plotted against principal components.25 Figure 9: Principal component plots for some of the major PC axes . 27 vi 1 Introduction 2 3 The crown clade Aves is a hugely diverse order (18,000+ species; Barrowclough et al., 4 2016) with a global distribution. Birds evolved from within maniraptoran theropods at 5 some point in the Cretaceous (Huxley 1868, Gauthier 1986), though it is still being 6 debated exactly which fossils are more closely related to birds than to other non-avialan 7 therapods (Xu et al. 2011, Turner et al. 2012, Agnolin & Novas 2013, Godefroit et al. 8 2013, Brusatte et al. 2014). Accordingly, they demonstrate dinosaurian and theropod 9 synapomorphies (Brusatte et al. 2014), with perforate acetabulae (Hutchinson 2001), 10 reduced numbers of digits (Xu & Mackem 2013), and retroverted pubes (Hutchinson 11 2001). The origin of flight within, or outside of the group remains hotly contested (Dyke 12 et al. 2013, Godefroit et al. 2013, Xu et al. 2015). The modern group has been able to 13 diversify into a huge number of ecological roles and niches across all continents and 14 oceans. 15 16 Prum et al. (2015) identify 14 major radiations within the modern clade of birds. Some of 17 these, e.g., Falconiformes, are dominated by a shared major hindlimb function, in this 18 case hunting and processing food (Ward et al. 2002, Struble & Organ 2016). Others, e.g., 19 Charadriiformes, possess a number of locomotor styles (Strauch 1978, Prum et al. 2015). 20 Most fundamentally, the clade is divided into two groups, the Paleognathae and the 21 Neognathae (Prum et al. 2015). The paleognaths are restricted today to the ratites and 22 tinamous, but several extinct groups existed (Davies & Bamford 2002). While they 23 represent the largest living taxa, the locomotor modes that they represent are restricted as 1 1 all of the modern groups are terrestrial, with many being entirely flightless (Davies & 2 Bamford 2002). Within paleognaths, only members of Tinamidae, the tinamous, retain 3 the ability to fly (Davies & Bamford 2002). Today, the neognaths are far more speciose, 4 representing the vast majority of extant bird taxa and ecological diversity (Prum et al. 5 2015). 6 7 Birds are active flyers, and accordingly possess several adaptations to deal with the 8 problems posed by flight: pneumatised skeletons allowing increased bone stiffness 9 without increasing mass (Currey & Alexander 1985), strut-like trabeculae (Rogers & 10 LaBarbera 1993) and, fused regions of the vertebral column (Baumel 1993). The flight 11 surface of birds is generated by the feathers of the wing. The leading edge is extended by 12 the primary feathers and the aerofoil cross-section is defined by the packing of the covert 13 feathers. The wing is stiffened chordwise by the rachis of the feathers and so needs no 14 trailing edge support (Rayner 1988). As a result, the hindlimb is not required to 15 contribute to the wing and so allows birds to have separate locomotor modules, with the 16 hindlimbs dedicated to non-volant locomotion and the wings to flight (Gatesy & Dial 17 1996). 18 19 As a highly speciose and globally ranging clade, birds show high morphological and 20 ecological disparity. Avian ecology and its role in the acquisition of flight have been 21 areas of scientific interest (Padian & Chiappe 1998, Hedenström 2002, Dececchi & 22 Larson 2011, Brusatte et al. 2015) since the description of Archaeopteryx (Owen 1863), 23 and many recent studies have used bird function to attempt to reconstruct the evolution of 2 1 flight (Dial 2003), to hypothesize the pre-flight function of feathers (Clarke 2013), or to 2 reconstruct the function of extinct stem or crown birds (Palmqvist & Vizcaíno 2003). 3 Many existing studies of avian limb allometry attempt to address questions in this last 4 category, either to develop datasets for reconstruction of wing variables from single 5 bones (Nudds 2007), to constrain flight capabilities (Vizcaíno & Fariña 1999, Chatterjee 6 et al. 2007), or to attempt to categorise ecology of extinct taxa (Bell & Chiappe 2011). 7 Avian body size has been shown to have consequences for clutch size (Price & Liou, 8 1989), brain size (Iwaniuk et al. 2004), and energy expenditure (McNab, 1994). 9 10 The large disparity in avian ecological traits has naturally attracted much research 11 attention towards understanding morphological adaptation for function (Rayner 1988, 12 Marsh & Dawson 1989, Worthington 1989, Hedenström 2002, Winger & Bates 2015, 13 Zhang et al. 2016), often with an eye to conservation of species (Green et al, 1989, Garcia 14 et al. 2017, Murgui & Hedblom 2017). Among these adaptational studies, a number seek 15 to find relationships between osteology and ecology, often for reconstruction of extinct 16 ecologies (Hinić‐Frlog & Motani 2010, Bell & Chiappe 2011, Field et al. 2013, Bell et al. 17 2019). Several studies (Warham 1977, Mönkkönen 1995, Hertel & Ballance 1999, Bell & 18 Chiappe, 2011, Zeffer et al. 2003, Hinić‐Frlog & Motani, 2010, Stoessel et al. 2013) have 19 established that avian ecology has an effect on the morphology of the limb skeleton, with 20 many (Zeffer et al. 2003, Reynaud 2006, Hertel et al. 2007, Endo et al. 2012, Stoessel et 21 al. 2013, Bell et al. 2019) focussing on the pelvic limb. This limb is less involved in flight 22 than the fore-limb, but has functions in reproduction (Dyke & Kaiser 2010) and non- 23 aerial locomotion. 3 1 2 The pelvis of birds demonstrates a tendency to recruit vertebrae from both the dorsal and 3 caudal segments of the spine into a complex synsacrum. They are fused, with ilia 4 extended both anteriorly and posteriorly, and strongly retroverted pubes (Iijima & 5 Kobayashi 2014). The bird femur has a trochanter and medially directed head (Baumel 6 1993), and sits inside a perforate acetabulum (Hutchinson 2001). The pelvis is ventrally 7 open, lacking midline symphyses (Baumel 1993, Dyke & Kaiser 2010). It is not well 8 understood which of these pelvic features are related to flight, and which to other 9 characteristics, such as oviparity. The avian pelvis has long been believed to differ in 10 shape between males and females due to the need for females to lay eggs (Dyke & Kaiser 11 2010), with egg shape correlating to pelvic shape (Shatkovska et al. 2018). It is known 12 that at least some taxa show sexual dimorphism in body size, and that this frequently 13 relates to reproductive strategy (Szekely et al. 2007). 14 15 16 Despite being such an active area of research, morphological research on the hindlimb of 17 birds has largely focussed on the long bones of the limb (Maloiy et al.