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Recognizing Sexual Dimorphism in the Fossil Record: Lessons from Nonavian Dinosaurs

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Recognizing Sexual Dimorphism in the Fossil Record: Lessons from Nonavian Dinosaurs Paleobiology, page 1 of 13 DOI: 10.1017/pab.2016.51 Recognizing sexual dimorphism in the fossil record: lessons from nonavian dinosaurs Jordan C. Mallon Abstract.—The demonstration of sexual dimorphism in the fossil record can provide vital information about the role that sexual selection has played in the evolution of life. However, statistically robust inferences of sexual dimorphism in fossil organisms are exceedingly difficult to establish, owing to issues of sample size, experimental control, and methodology. This is particularly so in the case of dinosaurs, for which sexual dimorphism has been posited in many species, yet quantifiable data are often lacking. This study presents the first statistical investigation of sexual dimorphism across Dinosauria. It revisits prior analyses that purport to find quantitative evidence for sexual dimorphism in nine dinosaur species. After the available morphological data were subjected to a suite of statistical tests (normality and unimodality tests and mixture modeling), no evidence for sexual dimorphism was found in any of the examined taxa, contrary to conventional wisdom. This is not to say that dinosaurs were not sexually dimorphic (phylogenetic inference suggests they may well have been), only that the available evidence precludes its detection. A priori knowledge of the sexes would greatly facilitate the assessment of sexual dimorphism in the fossil record, and it is sug- gested that unambiguous indicators of sex (e.g., presence of eggs, embryos, medullary bone) be used to this end. Jordan C. Mallon. Palaeobiology, Canadian Museum of Nature, Post Office Box 3663, Station D, Ottawa, Ontario K1P 6P4, Canada. E-mail: [email protected] Accepted: 21 November 2016 Data available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.8f6d2 Introduction Andersson 1994), so it is used here for strictly pragmatic reasons. Sexual dimorphism is broadly defined as the The semantic debate about sexual dimor- phenomenon in which the sexes of a species are phism has likewise sparked disagreement phenotypically different. Such differences typi- concerning what counts as evidence for sexual cally become more pronounced with maturity, selection. Assuming a strict definition of sexual and are usually manifested in the morphology dimorphism, only the documentation of dis- of the reproductive organs, but may also continuous character states counts toward an include variation in the shapes of display (e.g., argument for sexual selection (Padian and horns and crests) and feeding structures, in Horner 2011a,b, 2013, 2014a,b). However, color, in body size, and in behavior. Recent assuming sexual dimorphism sensu lato, the debate has centered on the semantics of sexual requirements are not nearly so strict, and a dimorphism, with some (Padian and Horner simple demonstration of positive allometry 2011a,b, 2013, 2014a,b) arguing that the term be may be admissible (Tomkins et al. 2010; Knell limited to describing discrete (presence/ et al. 2013b; Hone et al. 2016b). Positive absence) features, and others (Knell and allometry in the absence of dimorphism has Sampson 2011; Knell et al. 2013a,b; Mendelson been attributed to mutual sexual selection and Shaw 2013; Borkovic and Russell 2014) (Hone et al. 2012). arguing for a more inclusive definition that In spite of these prior disputes, what remains encompasses continuous variation. The latter uncontroversial is that sexual dimorphism definition is the more commonly and widely (however defined) typically results from sexual employed (e.g., Cunningham 1900; Schoener selection. Therefore, the identification of sexual 1967; Hedrick and Temeles 1989; Shine 1989; dimorphism in the fossil record can yield © 2017 The Paleontological Society. All rights reserved. 0094-8373/17 Downloaded from https:/www.cambridge.org/core. IP address: 97.115.205.50, on 30 Mar 2017 at 01:45:35, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2016.51 2 JORDAN C. MALLON important insights into the role that sexual dimorphic character, ideally more often than selection has played in the history of life. would be expected due to chance alone. Sexual dimorphism has, indeed, been attri- Issues of Control.—The ability to convincingly buted to various fossil metazoans, including demonstrate sexual dimorphism in the fossil trilobites (Knell and Fortey 2005), ammonites record is contingent on the control of (Callomon 1963), mammals (Van Valkenburgh confounding sources of variation, including and Sacco 2002), and birds (Chinsamy et al. interspecific and individual differences, 2013; Handley et al. 2016), among others ontogeny, taphonomic processes and (Westermann 1969). However, recognizing diagenesis, geography, and pathology. sexual dimorphism in fossil organisms is However, with few exceptions, this is rarely replete with difficulties, owing to the limita- done, leading to spurious claims of sexual tions of a priori sexual identification and issues dimorphism. Examples of such claims may of ruling out confounding sources of morpho- include instances of vertebral fusion logical variation. What follows is an investiga- (Rothschild and Berman 1991; Rinehart et al. tion into some of the common approaches used 2009) and variation in vertebral count (Galton to identify sexual dimorphism in the fossil 1999), both of which are known to vary record, using nonavian dinosaurs (hereafter, individually in modern taxa (Danforth 1930; simply “dinosaurs”) as a study model. Dating Asher et al. 2011; VanBuren and Evans in back to the early considerations of Nopcsa press). Claims of sexual dimorphism in (1929), dinosaurs have featured prominently in ceratopsids (Sternberg 1927; Lehman 1990) discussions about sexual dimorphism in the and hadrosaurids (Nopsca 1929; Dodson fossil record (Chapman et al. 1997; Isles 1975; Hopson 1975; Weishampel 1981) have 2009; Dodson 2011; Table 1) and serve to been shown to be untenable due to the highlight the methodological shortcomings stratigraphic isolation of the dimorphs, underpinning many common approaches. suggesting species differences instead (Ryan These issues are briefly discussed in the and Evans 2005; Evans 2007; Mallon and following sections, before a more rigorous Holmes 2006). Ontogeny is particularly approach is presented. This approach reveals important to consider, because individuals just how difficult it can be to detect sexual can continue to gain mass even after having dimorphism in the fossil record, and highlights reached skeletal maturity, conceivably the need for more integrative approaches resulting in size dimorphism (Padian and going forward. Horner 2013). Many studies account for Issues of Sample Size.—Sample size matters ontogeny using a superficial age proxy (e.g., when attempting to positively identify sexual body size, osteological fusion, bone surface dimorphism in a fossil species (Rozhdestvensky texture), but none of these proxies are foolproof 1965; Plavcan 1994; Kościński and Pietraszewski (Hone et al. 2016a). No study of sexual 2004). Some purported examples of sexual dimorphism in dinosaurs to date has dimorphism in fossil taxa have relied on incorporated skeletochronological age sample sizes of just two (e.g., Sternberg 1927; determination; those studies that have Carpenter et al. 2011; Persons et al. 2015). determined the skeletochronological age of However, given that no two individuals are specimens (e.g, Horner and Padian 2004; exactly alike, it is a truism that two individuals Klein and Sander 2007; Woodward et al. 2015) will be dimorphic. Many more alleged have not identified gross skeletal features that examples of sexual dimorphism are based on would help to establish the sex to which the sample sizes of less than 10 (e.g., Gingerich specimens belonged. 1981; Deng 2005; Sanchez et al. 2010; Lü et al. Issues of Methodology.—A problem common 2011; Table 1), which is insufficient for statistical to many quantitative studies of fossil taxa is purposes (Kościński and Pietraszewski 2004). that they inherently assume dimorphism rather To validate the dimorphism hypothesis, a than test for it. This is true of some of the most sample must be composed of multiple common and widely advocated methods used specimens that consistently express the for detecting sexual dimorphism in Downloaded from https:/www.cambridge.org/core. IP address: 97.115.205.50, on 30 Mar 2017 at 01:45:35, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2016.51 at Downloaded from https:/www.cambridge.org/core/terms TABLE 1. Purported examples of sexual dimorphism in the fossil record of Dinosauria. Asterisk (*) denotes study formally reevaluated here. Abbreviations: ANOVA, analysis of variance; MANOVA, multivariate analysis of variance; PCA, principal components analysis; PCO, principal coordinates analysis; RMA, reduced major axis regression. https:/www.cambridge.org/core Discrete or continuous Parent taxon Species Purported dimorphic character(s) character(s)? n Methods Reference Coelophysidae Coelophysis bauri Skull length, neck length, forelimb length, Continuous, discrete None Colbert (1989, 1990) fusion of sacral neural spines Skull length, neck length, fusion of sacral Continuous, discrete 122 Regression analysis, Rinehart et al. (2009)* vertebrae 4 + 5, femur head width analysis of variance C. (‘Syntarsus’) Femoral lesser trochanter shape Continuous >30 Bivariate plots Raath (1990)* rhodesiensis . https://doi.org/10.1017/pab.2016.51
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