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Cope's Rule in the Pterosauria, and Differing doi: 10.1111/j.1420-9101.2006.01284.x Cope’s Rule in the Pterosauria, and differing perceptions of Cope’s Rule at different taxonomic levels D. W. E. HONE* &M.J.BENTON* *Department of Earth Sciences, University of Bristol, Bristol, UK Bayerische Staatssammlung fu¨ r Pala¨ontologie und Geologie, Mu¨ nchen, Germany Keywords: Abstract Cope’s Rule; The remarkable extinct flying reptiles, the pterosaurs, show increasing body giantism; size over 100 million years of the Late Jurassic and Cretaceous, and this seems macroevolution; to be a rare example of a driven trend to large size (Cope’s Rule). The size Pterodactyloidea; increases continue throughout the long time span, and small forms disappear Pterosauria; as larger pterosaurs evolve. Mean wingspan increases through time. Exam- Rhamphorhynchoidea. ining for Cope’s Rule at a variety of taxonomic levels reveals varying trends within the Pterosauria as a whole, as pterodactyloid pterosaurs increase in size at all levels of examination, but rhamphorhynchoid pterosaurs show both size increase and size decrease in different analyses. These results suggest that analyses testing for Cope’s Rule at a single taxonomic level may give misleading results. feature of many lineages, or just a rare and unusual Introduction occurrence, and to clarify that simple size increase Many clades show increasing body size through time, a through time is not in itself enough to warrant special phenomenon often loosely called Cope’s Rule (Benton, explanation. 2002). This has been a part of evolutionary biology Large size is expected to convey certain advantages in theory for over a century (Cope, 1896), yet it has never both interspecific and intraspecific competition (Schmidt- gained common acceptance. It has been demonstrated to Nielsen, 1984; Benton, 2002; Hone & Benton, 2005) and operate in some groups (Arnold et al., 1995; Poulin, thus Cope’s Rule might be expected to be observed 1995; Alroy, 2000) but not in others (Jablonski, 1997; widely, yet this is apparently not the case. Counter Gould & McFadden, 2004; Moen, 2006), and yet Cope’s selection for smaller size should appear when size limits Rule has been dismissed by some as imaginary, either an are achieved or ecological pressures are applied, e.g. artefact of passive evolution (small ancestors can only limits on resources, dramatic environmental change, produce similar-sized or larger descendants; Stanley, competition from superior, larger species etc. (Kingsolver 1973), an increase in variance (where small forms & Pfennig, 2004; Hone & Benton, 2005) but within a remain as part of the evolving clade, and larger forms context of general size increase. Apparent variation in are added as the clade becomes more diverse), rather selection pressures may be partly a result of testing for than a uniform driven trend (Gould, 1988), or even Cope’s Rule at differing levels of phylogeny. As Alroy psychological (‘bigger is better’; Gould, 1997). However, (2000) showed, large-scale trends like Cope’s Rule may Cope’s Rule has recently attracted much attention only be apparent at certain phylogenetic levels. Short- (Knouft & Page, 2003; Kingsolver & Pfennig, 2004; term or low-level trends may be masked over extended Laurin, 2004; Webster et al., 2004; Hone & Benton, 2005; periods of time or at high phylogenetic levels (as seen in Hone et al., 2005; Hunt & Roy, 2006; Moen, 2006) and some dinosaurian clades in Hone et al., 2005). Similarly, merits further investigation to determine whether it is a analyses over short time periods or at low taxonomic levels may miss large-scale trends that take millions of Correspondence: David W. E. Hone, Bayerische Staatssammlung fu¨ r years to become apparent. Therefore there remains an Pala¨ontologie und Geologie, Richard-Wagner-Straße 10, D-80333 Mu¨ nchen, Germany. apparent conundrum: even if Cope’s Rule is detected, is it Tel.: +49 (0)89 2180 6613; fax: +49 (0)89 2180 6601; a true evolutionary effect, or merely a medium-term e-mail: [email protected] pattern not seen over shorter or longer time spans? ª 2007 THE AUTHORS 20 (2007) 1164–1170 1164 JOURNAL COMPILATION ª 2007 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY Cope’s Rule in pterosaurs 1165 Pterosaurs were the first vertebrates to achieve even the most disparate wing shapes of pterosaurs are powered flight and so represent an important part of still very similar. Furthermore, wingspan must correlate vertebrate evolutionary history. Although pterosaur with body mass, as the amount of lift generated by the remains are relatively scarce compared with their large- wings must be sufficient to maintain flight. However, two bodied contemporaries, the dinosaurs and marine factors could complicate this rather simple assumption. reptiles, they represent an important component of First, in larger pterosaurs, a reduction in the thickness of Mesozoic faunas as the only flying vertebrates for long bones allowed for an increase in overall weight 60 million years (Myr) (Unwin, 2006). without an increase in wingspan (Bonde & Christiansen, Pterosaurs consist of many families in two major 2003). Secondly, the pterodactyloids also reduced their suborders – the paraphyletic ‘Rhamphorhynchoidea’ net wing area per unit length, as the main flight wing, (relatively small, with a long tail, from the Late Triassic the cheiropatagium, was probably attached to the knee, to the Early Cretaceous) and the Pterodactyloidea (rel- and not the ankle as in rhamphorhynchoids (Bennett, atively large, reduced tail, from the mid-Jurassic to the 2000). However, these differences may be ignored in end Cretaceous) (Wellnhofer, 1991). As flying organ- within-family comparisons, and comparisons between isms, their body sizes must have been constrained by the families will involve relatively large differences and so aerodynamic demands of flight (Alexander, 1998). Even the results should not be affected. so, pterosaurs include the largest flying organism so far In most cases, complete wing specimens were used, but known – Quetzalcoatlus with a wingspan of 12 m on occasion missing terminal phalanges were scaled from (Wellnhofer, 1991, pp. 142–143), and their minimum close relatives. Single wings can be doubled in total length size was large compared with both birds and bats: to provide an estimate for total wingspan. Although the Jeholopterus spanned 0.35 m (Wang et al., 2002). Smaller width of the torso is missing from this estimate, the elbow nonadult records include a young Pterodactylus with a would naturally be flexed, so reducing the total wingspan. wingspan of just 0.18 m (Wellnhofer, 1991, p. 88) and Thus the underestimate for the missing body is balanced new evidence suggests that even tiny, newly hatched by the overestimate of measuring the total length of all pterosaurs could fly (Wang & Zhou, 2004; Unwin, 2006). forelimb bones. This simple doubling of the total length of Pterosaurs have attracted a great deal of interest the wing bones therefore provides an accurate represen- recently, with considerable effort devoted to their origins tation of the actual wingspan of the animal in life (Bennett, 1996; Peters, 2000), phylogenetics, (Kellner, (Bennett, 2001). Pterosaurs do show variation in the 2003; Unwin, 2003) and biology (Bennett, 2001; Bonde scaling of the bones that make up the wing (Hazlehurst, & Christiansen, 2003; Frey et al., 2003; Wilkinson et al., 1991) but these are constrained within both families and 2006). Pterosaurs are represented by many complete genera, and so estimates are adequate for comparison of specimens and they were diverse, with approximately 60 closely related taxa. genera in 20 families (Unwin, 2003, 2006). The aim of Pterosaur nomenclature used here is based on the this paper was to assess whether or not pterosaurs show revisions by Unwin (2003). Measurements were collec- evidence of Cope’s Rule. Coupled with this analysis is an ted from the literature and from other researchers, and, investigation into the effects of testing for Cope’s Rule at where possible, these measures were taken from multiple different phylogenetic levels based on the pterosaurs. sources to corroborate and cross check the methods. The data are presented in Appendix S1 (see Supplementary Materials and methods Material), with sources. Slack et al. (2006) have carried out a superficially similar analysis of pterosaur wingspan, In order to test for the presence of Cope’s Rule, both but not directed at assessing the validity of Cope’s Rule. within a single lineage and across multiple lineages, a Their data set is larger than ours, but it includes a high measure of body size, and ancestor/descendant relation- number of invalid taxa and incomplete specimens, and ships must be established. Testing must also be performed the basis for some of the wingspan estimates is not clear. at an appropriate taxonomic level, as testing at high levels Putative ‘ancestor-descendant’ pairs may be deter- (e.g. families) may miss generic-level trends (Alroy, 2000, mined from stratigraphy (e.g. Alroy, 1998), or from a and corroborated by Kingsolver & Pfennig, 2004). phylogeny (e.g. Hone et al., 2005). For pterosaurs, most Determining body mass accurately for extinct organ- published phylogenies are characterized by large ghost- isms is very difficult, so most authors have used an easily lineages (times when the taxon was assumed to exist from measured morphological feature as a proxy for body evidence of its phylogenetic affinities, but for which no mass. For example, Alroy (1998) used molar tooth size fossils are known) and therefore family groups were for mammals, Jablonski (1997) used shell height and established using phylogenetic analysis, and within-fam- length for molluscs, and Moen (2006) used carapace ily ‘ancestor/descendant’ pairs were then based on strat- length in turtles. Here, total wingspan is used as a proxy igraphic differences. Of the available, recent, complete for body mass in pterosaurs. pterosaur phylogenies, that of Unwin (2003) was chosen In pterosaurs, the wing shape was far more constrained as being the most suitable for this analysis.
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