Dimorphism has been reported in every major dinosaur clade and has often been attributed to sex-specific variation (Dodson, 1975; Chapman et al., 1997; Bunce et al., 2003; Padian and Horner, 2011; Knell and Sampson, 2011; Knell et al., 2013; Mallon, 2017; Saitta et al., 2020). However, recent studies have demonstrated that most of the documented cases of sexual dimorphism in extinct dinosaurs were most likely biased by ontogenetic changes, taphonomic deformations, and small sample sizes, which substantially affect the representativeness of the inter- and intraspecific diversity and undermine statistical analyses (Griffin and Nesbitt, 2016; Hone et al., 2017; Saitta et al., 2020). For example, a discrete and binary variation between gracile and robust morphologies of femoral bone scars, mostly at the level of the lesser trochanter, has frequently been inferred, with more or less confidence, as sexual dimorphism in various ceratosaurian theropods and non-dinosaurian dinosauriforms (Colbert, 1990; Raath, 1990; Benton et al., 2000; Britt and Chure, 2000; Piechowski et al., 2014). More recently, Griffin and Nesbitt, 2016 demonstrated that this feature no longer appeared dimorphic when accounting for ontogenetic series in the silesaurid Asilisaurus. In addition, it has been demonstrated on modern populations that sexual dimorphism could be represented only by very subtle morphological variations, making it even harder to detect in fossils with smaller sample sizes (Hone et al., 2020; Saitta et al., 2020). At a larger scale, Mallon, 2017 performed a statistical investigation on a large set of studies that hypothesized sexual dimorphism based on a wide diversity of anatomical proxies across the major clades of non-avian dinosaurs. However, among the 48 described occurrences, only 9 datasets were suitable for statistical test, among which only 1 was considered to rigorously demonstrate dimorphism. Indeed, the combination of a principal component analysis (PCA) and a mixture modeling analysis highlighted that the shift in posterior inclination between the eighth and ninth dermal plates of Stegosaurus mjosi was best explained by a bimodal distribution. Yet, there is not robust evidence to postulate that the dimorphism shown in dermal plates would be sex specific (Saitta, 2015). As a consequence, it appears that no dataset has yet rigorously demonstrated the presence of sexual dimorphism in non-avian dinosaurs (Hone et al., 2020). According to Mallon, 2017, one should review three issues when demonstrating sexual dimorphism on extinct organisms: (1) sample size in order to ensure population representativeness; (2) methodology in order to use only suitable analyses to study sexual dimorphism, such as mixture modeling; (3) any other intraspecific morphological variation such as ontogeny and pathology, as well as taphonomy.

Here, we studied the intraspecific femoral variation among a remarkably dense and well preserved population of ornithomimosaurs (Allain et al., 2014, Allain et al., 2022) from the Angeac-Charente Lagerstätte (Lower Cretaceous of France). Rozada et al., 2014 and Rozada et al., 2021 demonstrated that at least 61 ornithomimosaur individuals belonged to the same herd and were deposited in a mass mortality event relying on several evidences (e.g. very limited transport; quality of bone preservation; abundance of individuals with a high skeletal representation preserved in a restricted spatial distribution; catastrophic age profile of the group; deposition of sediment and bones under coeval, poorly oxygenated burial and diagenesis conditions given by their rare earth elements and Yttrium profiles). Thus, the ornithomimosaur herd of Angeac-Charente represents a unique occasion to study subtle parameters such as intraspecific variation in extinct dinosaurs. Moreover, the exceptionally high minimal number of individuals among the herd, represented by tibiae and femora (Table 1), offers a singular opportunity to test for the presence of dimorphism and characterize its variation. Indeed, and in addition of being the most abundant bones discovered from the Angeac-Charente ornithomimosaur, many hypotheses of sexual dimorphism were formulated based on the hindlimb morphology of non-avian dinosaurs (Colbert, 1990; Raath, 1990; Larson, 1994; Benton et al., 2000; Britt and Chure, 2000; Carrano et al., 2002; Bunce et al., 2003; Piechowski et al., 2014) but also observed in extant archosaurs (Schnell et al., 1985; Farlow et al., 2005; Charuta et al., 2007; Bonnan et al., 2008; Elzanowski and Louchart, 2022).

We used a 3D geometric morphometric (3D GM) approach that combines anatomical landmarks and sliding semilandmarks along curves and surfaces on both complete and fragmented femora and tibiae (Figure 1—figure supplement 1A–B; Gunz et al., 2005; Gunz and Mitteroecker, 2013). This method is well suited to study biological objects, including limb bones, and to detect subtle intraspecific shape variations (Zelditch et al., 2012; Botton-Divet et al., 2016) such as dimorphism (Fabre et al., 2014). We then investigated the resulting dataset using PCAs and Gaussian mixture modeling (GMM) as clustering analyses. This clustering analysis calculates the number of Gaussian distributions present in a dataset by maximum likelihood estimations and has been demonstrated as a well-suited method for the identification of dimorphism (Godfrey et al., 1993; Dong, 1997; Fabre et al., 2014; Manin et al., 2016; Mallon, 2017; Saitta et al., 2020).

We highlight a dimorphic variation in femora from the ornithomimosaur herd of Angeac-Charente (Figure 1A–B). This dimorphic variation is localized along the diaphysis (i.e. lateromedial curvature) and toward the distal epiphysis (i.e. lateromedial width) of the femur (Figure 1C–D). Distributions along the PC1 of complete femora (28.8%) and distal epiphyses (27.9%) are best described by two clusters with a ratio close to 1:1 according to GMM analyses (see Supplementary file 1 for details). PC1 scores from both analyses are not significantly correlated to the log centroid size, indicating that size-related effects have no impact on the observed dimorphism (p-value>0.1 for complete femora and distal epiphyses, Supplementary file 1).

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The most important morphological variation of complete femora is a medial to lateral curvature of the femur (Figure 1C). The proximal third of the femur appears deviated toward the lateral side in specimens on the negative part of the PC1 axis, whereas specimens located on the positive part have straight to medially curved femora (Figure 1C). Coincidentally, the femoral head is directed medially in the negative cluster while it is inclined ventromedially in the positive one (Figure 1C). Regarding distal epiphyses, we selected 6 (out of 10) epiphyses from complete femora because the other 4 were taphonomically altered or pyrite encrusted only in the distal area, which would appear relatively more important in analyses restricted only to this area rather than on the complete morphology (Supplementary file 2). Nevertheless, for distal epiphyses, the most important morphological variation along PC1 is the expansion of the lateromedial width relative to the anteroposterior length, which is greater in specimens on the positive part of the PC1 axis than on the negative one (Figure 1D). In addition, we highlight that the 6 distal epiphyses from complete femora are consistently attributed to the same clusters between the two analyses (Figure 1A, B; Supplementary file 2). Hence, our study shows that the straighter the shaft is, the more robust the epiphysis is and that this relationship is dimorphic.

However, there is no robust bimodal distribution on proximal epiphyses, as shown by the GMM analyses (Figure 1—figure supplement 2; no consistency in the specimen attribution between complete femora and proximal epiphyses). Similarly, there is no dimorphism in the morphological variation of complete tibiae (Figure 1—figure supplement 3) along PC1 (24.1%) and PC2 (20.0%).

The closest extant relatives of non-avian dinosaurs are known to display sexual dimorphism with more or less visibility: birds display variation in their plumage and skeleton (Schnell et al., 1985; Owens and Hartley, 1998; Dunn et al., 2001; Székely et al., 2007; Clarke, 2013; Duggan et al., 2015; Manin et al., 2016; Hone et al., 2017; Elzanowski and Louchart, 2022), whereas the variation is restricted to the skeleton in crocodilians (Fitch, 1981; Farlow et al., 2005; Cox et al., 2007; Prieto-Marquez et al., 2007; Bonnan et al., 2008; Hone et al., 2017; Hone et al., 2020). The extant phylogenetic bracket (EPB) of non-avian dinosaurs (Witmer, 1995) thus implies they were sexually dimorphic too (Hone et al., 2017; Hone et al., 2020).

A femoral dimorphism of the same nature was demonstrated to be sex-specific among populations of extant tetrapods such as carnivorans and primates. Dimorphism in the femoral obliquity (also termed ‘bicondylar angle’) was observed in humans, for which females had higher angles than males (Parsons, 1914; Tardieu et al., 2006; Hunt et al., 2021). Moreover, a higher lateromedial width of the distal epiphysis (also termed ‘epicondylar width’ or ‘bicondylar breadth’) was demonstrated to vary between sexes in gray wolves and other carnivorans, as well as in primates (Alunni-Perret et al., 2008; Gaikwad and Nikam, 2014; Morris and Brandt, 2014; Cavaignac et al., 2016; Morris and Carrier, 2016). Whereas no similar sexual dimorphism had been shown – or studied – in non-archosaurian sauropsids to our knowledge, many relevant examples are available in extant and sub-fossil archosaurs. A higher distal width in males than females was demonstrated in wild and captive Alligator mississippiensis using linear and geometric morphometrics (Farlow et al., 2005; Bonnan et al., 2008). Handley et al., 2016 demonstrated that femoral distal width of the more recently extinct flightless bird Dromornis stirtoni was also higher in males than females. To do so, they coupled morphometrics and multivariate statistics with the observation of medullary bone, a sex-specific tissue present in bones of egg-laying female in archosaurians (Dacke et al., 1993; Schweitzer et al., 2005; Schweitzer et al., 2007; Canoville et al., 2019). The same kind of sexual dimorphism was observed in modern birds like California gulls (Larus californicus; Schnell et al., 1985) and in the two extant species of ostriches (Struthio c. camelus and S. c. molybdophanes) but with reversed proportions between males and females (Elzanowski and Louchart, 2022). Furthermore, Duggan et al., 2015 demonstrated that young male domestic ducks (Anas platyrhynchos) had more laterally curved femora than females and that this sexually dimorphic feature disappeared along ontogeny. However, to our knowledge and aside from Duggan et al., 2015, data about femoral obliquity is generally unavailable in most studies including sex determination in birds and other sauropsids. Therefore, because the femoral dimorphic features we highlighted in the Angeac-Charente ornithomimosaur herd were also demonstrated to vary between sexes in more or less closely related extant vertebrate clades, we infer it to be sexual.

Ontogenetic allometry was often misinterpreted as sexual dimorphism in archosaurs, as demonstrated in the early dinosauriform Asilisaurus kongwe, the crocodylian A. mississippiensis and the bird Rhea americana (Griffin and Nesbitt, 2016; Hone et al., 2017; Hedrick et al., 2022). However, we found no allometry along the first PC axis (Supplementary file 1), which, in addition of rejecting ontogenetic allometry, indicates that the dimorphism is not related to size, as suspected by the homogeneity of femoral lengths highlighted in Supplementary file 3 among complete femora. Therefore, this indicates no sexual size dimorphism (SSD) in the femur of the Angeac-Charente ornithomimosaurs. SSD is one of the most documented sexual dimorphism across all living organisms, whether it is biased toward females or males (Darwin, 1874; Fairbairn et al., 2007). There are many examples of observations and/or inferences of SSD and allometric relationships in extant and extinct dinosaurs (Larson, 1994; Bunce et al., 2003; Clarke, 2004; Székely et al., 2007; Remeš and Székely, 2010; Olson and Turvey, 2013; Handley et al., 2016; Manin et al., 2016; Fajemilehin, 2017). However, Elzanowski and Louchart, 2022 demonstrated that female ostriches had more robust limb bones but smaller average body size than males. This decoupling between size and shape dimorphism is concordant with our results and emphasizes that sexual dimorphism is not necessarily reflected by body size or allometry between limb segments. Thus, size-independent sexual dimorphism should be investigated further extant archosaurs in order to improve inferences about sexual dimorphism in fossils, which are most often represented only by isolated bones.

We did not identify any other dimorphism in either the proximal part of the femur or in complete tibia of the Angeac-Charente ornithomimosaurs (Figure 1—figure supplements 2 and 3). However, sexual dimorphism was observed in the proximal ends of femora in extant ostriches (Charuta et al., 2007; Elzanowski and Louchart, 2022) and California gulls (Schnell et al., 1985). In addition, the anteroposterior width of the femoral shaft was demonstrated to vary between sexes among savannah sparrows (Passerculus sandwichensis; Rising, 1987) and three species of steamer-ducks (Tachyeres pteneres, Tachyeres leucocephalus, and Tachyeres patachonicus; Livezey and Humphrey, 1984). Yet, and accordingly with our results, size-independent dimorphism in the avian tibiotarsus seems less common across the EPB. Indeed, to our knowledge, occurrences of shape dimorphism in the tibia was demonstrated only in California gulls (e.g. width of the shaft; Schnell et al., 1985) and in ostriches (e.g. anteroposterior width of the distal epiphysis; only in Elzanowski and Louchart, 2022 but not in Charuta et al., 2007). Furthermore, our observation that sexual dimorphism could be restricted to the femur in the Angeac-Charente ornithomimosaurs and modern archosaurs raises the question of the potential co-variation between the femur and the pelvis. Sexual dimorphism was observed in the ilium of several birds mentioned previously, such as ostriches, steamer-ducks, savannah sparrows, and California gulls (in the antitrochanter width, acetabular width, and synsacrum width and length; Livezey and Humphrey, 1984; Schnell et al., 1985; Rising, 1987; Charuta et al., 2007). All measurements were higher in male birds than in female birds except for the width of the ilium, which was higher in female ostriches when measured by Charuta et al., 2007 but not significantly different between sexes in Elzanowski and Louchart, 2022. Additionally, female alligators had a deeper pelvic canal (i.e. distance between the ventral side of the first sacral vertebra and the ventral margin of the ischial symphysis; Prieto-Marquez et al., 2007). The dimorphism was located preferably on the femur rather than on the tibia in the Angeac-Charente ornithomimosaur, which suggests that the pelvic area might as well be dimorphic and that seems to be generally the case in some modern avian dinosaurs too (Livezey and Humphrey, 1984; Schnell et al., 1985; Rising, 1987; Farlow et al., 2005; Charuta et al., 2007; Prieto-Marquez et al., 2007; Bonnan et al., 2008; Duggan et al., 2015; Elzanowski and Louchart, 2022). Could the ability to carry eggs restrict the location of sexual dimorphism closer to the hip region? Sexual dimorphism in the pelvic girdle, the proximal hindlimb and the morphological integration between the two in female extant archosaurs should be investigated further to answer this question. However, one would expect that dimorphism in the pelvic morphology would correlate with dimorphism in the proximal instead of the distal femoral portions. Perhaps the shaft curvature toward the lateral side of the femur could have enabled ornithomimosaurs with a wider pelvis (presumably female individuals) to retain their hindlimbs close to the sagittal midline. Nevertheless, the current dataset does not allow to further speculate without the possibility to sex each morphotype and without the integration of femoral with pelvic data.

Our results did not permit to confidently sex each morphotype. Most modern occurrences of femoral sexual dimorphism indicate a wider distal epiphysis among males than females, but Elzanowski and Louchart, 2022 showed that the opposite was also true for modern and subfossils ostriches. Furthermore, our results indicated that femora with the narrowest distal epiphyses (females in most of modern occurrences) had a laterally deviated shaft. However, Duggan et al., 2015 demonstrated that only juvenile male Pekin ducks had a laterally deviated shaft, which is not congruent with our results that the widest epiphyses were associated with a straighter morphotype. Paleohistological analyses could enable to verify sex assignment by assessing the presence of medullary bone, as some gravid females may have died during their egg-laying cycle at the time of the mass-mortality event recorded at Angeac-Charente. Indeed, medullary bone was recently demonstrated as probably the most reliable indicator of sex with an extensive distribution across the skeleton (Canoville et al., 2019). A paleohistological investigation could also confirm the ontogenetic homogeneity among our femoral sample, as recommended by Griffin and Nesbitt, 2016, Hone et al., 2017 and Mallon, 2017.

Specimens used in this study are housed in the collections of the Angoulême Museum, Angoulême, France and are available under demand. 3D models used in this study are shared freely and publicly on MorphoSource.

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Author details

1. Romain Pintore

   1. UMR 7179, Mécanismes Adaptatifs et Évolution (MECADEV), Muséum National d’Histoire Naturelle, CNRS, Paris, France
   2. Structure and Motion Laboratory, Department of Comparative Biomedical Sciences, Royal Veterinary College, Hatfield, United Kingdom

   Contribution

   Resources, Software, Formal analysis, Investigation, Visualization, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   romain.pintore@edu.mnhn.fr

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2438-614X

2. Raphaël Cornette

   UMR 7205, Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, UA, Paris, France, Paris, France

   Contribution

   Supervision, Investigation, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

3. Alexandra Houssaye

   UMR 7179, Mécanismes Adaptatifs et Évolution (MECADEV), Muséum National d’Histoire Naturelle, CNRS, Paris, France

   Contribution

   Conceptualization, Supervision, Funding acquisition, Investigation, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8789-5545

4. Ronan Allain

   UMR 7207, Centre de Recherche en Paléontologie - Paris (CR2P), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, Paris, France

   Contribution

   Conceptualization, Data curation, Supervision, Funding acquisition, Validation, Methodology, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6357-1586

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