[The final published version of this article is available online. Please check the final publication record for the latest revisions of this article: Cullen, T. M., Fraser, D., Rybczynski, N. and Schröder-Adams, C. (2014), Early evolution of sexual dimorphism and polygyny in Pinnipedia. Evolution, 68: 1469–1484. doi:10.1111/evo.12360] Early evolution of sexual dimorphism and polygyny in Pinnipedia Thomas M. Cullen1,*, Danielle Fraser2, Natalia Rybczynski3, Claudia Schröder-Adams1 1Department of Earth Sciences, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1S 5B6, Canada 2Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario K1S 5B6, Canada 3Palaeobiology, Canadian Museum of Nature, PO Box 3443 Stn ‘D’, Ottawa, Ontario K1P 6P4, Canada Key Words: Fossil; Mating Systems; Coevolution, Miocene; Phocidae; Otariidae; Reproductive Strategies Total words (not including figure captions, literature cited): 6977 Tables: 0. Figures: 8 All data included as supplementary information T. M. Cullen et al. !1 * Correspondence and requests for materials should be addressed to T.M.C. (current address: [email protected], Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada). Running Header: Cullen et al. — Evolution of sexual dimorphism in pinnipeds Abstract Sexual selection is one of the earliest areas of interest in evolutionary biology. And yet, the evolutionary history of sexually dimorphic traits remains poorly characterized for most vertebrate lineages. Here we report on evidence for the early evolution of dimorphism within a model mammal group, the pinnipeds. Pinnipeds show a range of sexual dimorphism and mating systems that span the extremes of modern mammals, from monomorphic taxa with isolated and dispersed mating to extreme size dimorphism with highly ordered polygynous harem systems. In addition, the degree of dimorphism in pinnipeds is closely tied to mating system, with strongly dimorphic taxa always exhibiting a polygynous system, and more monomorphic taxa possessing weakly polygynous systems. We perform a comparative morphological description, and provide evidence of extreme sexual dimorphism (similar to sea lions), in the Miocene-aged basal pinniped taxon Enaliarctos emlongi. Using a geometric morphometric approach and combining both modern and fossil taxa we show a close correlation between mating T. M. Cullen et al. !2 system and sex-related cranial dimorphism, and also reconstruct the ancestral mating system of extant pinnipeds as highly polygynous. The results suggest that sexual dimorphism and extreme polygyny in pinnipeds arose by 27 Ma, in association with changing climatic conditions. Introduction Charles Darwin wrote extensively about the evolution of behavioural and morphological differences between the sexes or sexual dimorphism (Darwin 1871). Morphological sexual dimorphism is manifested as differences in size or shape, including ornamentation, between the sexes of a given species, some of which are preserved in the fossil record. The occurence of sexual dimorphism (SD) has been reported numerous times in the vertebrate fossil record (e.g. sharks, ungulates, carnivorans, turtles, dinosaurs) (Janis 1982; Lund 1985; Chapman et al 1997; Carrano et al 1999; Mead 2000; Playcan 2000; Deméré and Berta 2002; Playcan 2012) and yet, the evolutionary history of such sexually dimorphic traits remains generally uninvestigated for most lineages (Hendrick and Temeles 1989). Understanding the evolution of sexual dimorphism (e.g. how and when does it arise?), which is often in opposition to Darwinian natural selection, is one of the original problems posed to evolutionary biologists, and has important implications for our understanding the coevolution of behavior (e.g. mating system) and intraspecific dimorphism (Leutenegger and Kelly 1977; Hendrick and Temeles 1989). For example, studies of ungulates suggest a strong association between SD and mating system; early T. M. Cullen et al. !3 fossil forms were generally monogamous and monomorphic, with dimorphism and polygyny evolving later in conjunction with the expansion of open grassland environments (Janis 1982; Pérez-Barbería et al 2002). Within primates, sexual dimorphism in body and canine size are related to male intra-sexual selection and can be used to infer polygyny in extinct taxa (Leutenegger and Kelly 1977; Playcan 2000). Such correlated evolution between morphology and behaviour, if present in other taxa, can be used to reconstruct and constrain inferences of the evolutionary history of sexually selected traits, and better predict their phylogenetic distribution (Playcan 2000; Playcan 2012). Tracing the evolution of SD along a phylogeny can allow us to reconstruct the evolutionary history of mating systems, giving us a better understanding of the timing of major morphological shifts and provide context for the origins of behavior and ecology seen in modern taxa (Weckerly 1998; Cassini 1999; Playcan 2000). Pinnipeds possess a wide range of reproductive strategies and sexual dimorphism, encompassing the extremes observed in modern mammals (Bartholomew 1970; Weckerly 1998; Naughton 2012). Otariids+odobenids display considerable SSD, a highly polygynous harem-based mating system, and a preference for land-based breeding (Bartholomew 1970; Cassini 1999; Lindenfors et al 2002). In contrast, almost all phocids display promiscuity with weak polygyny, a preference for breeding in the water or on ice floes, and relatively little sexual size dimorphism (SSD) (Bartholomew 1970; Cassini 1999; Lindenfors et al 2002). The exceptions to this are three derived and phylogenetically distant genera, Halichoerus and Mirounga, which appear to converge on more otariid-like dimorphism and behaviour (harem-based land breeding), and T. M. Cullen et al. !4 Cystophora, which exhibits noticeable SSD, and form otariid-like breeding colonies (though on ice floes, not shore) (Fig. 1) (Cassini 1999; Naughton 2012; Nyakutura and Bininda-Emonds 2012). Water or ice-based mating occurs in taxa (i.e. most phocids) living in primarily higher latitude waters with greater primary productivity, whereas colony forming taxa (i.e. otariids) live in comparably lower latitude waters with lower productivity (Ferguson and Higdon 2006; Jones and Goswami 2010B). It has been suggested that environmental factors, particularly ocean productivity, have been an important driver of the evolution of the form and mating system of modern pinnipeds (Ferguson and Higdon 2006). Given that, with few exceptions, phocids and otariids+odobenids display disparate reproductive strategies (and patterns of SSD) it is impossible to reconstruct the ancestral condition of SSD in crown pinnipeds based solely on modern taxa. There is some evidence that SSD may have deep origins within Pinnipedia; desmatophocids (e.g. Desmatophoca, Allodesmus), an extinct sister clade to the phocids, show SSD (Deméré and Berta 2002). However, the phylogenetic position of desmatophocids is after the divergence of phocids and otariids+odobenids (Boessenecker and Churchill 2013) (Fig. 1), contributing little to the study of SSD evolution among early pinnipeds; SSD was either lost in phocids (and later regained in two modern genera) or occurred in desmatophocids as a result of parallel evolution with otariids+odobenids. Here, we use a combination of evidence from fossil and modern taxa to reconstruct the ancestral mating system of pinnipeds. We include material of the late Oligocene to early Miocene-aged (~27-20 Ma) fossil taxon Enaliarctos, an intermediate T. M. Cullen et al. !5 form regarded as an outgroup to crown pinnipeds (Berta and Adam 2001; Bebej 2009), and therefore important for reconstructing ancestral states. Unlike the freshwater, web- footed fossil taxon Puijila darwini (Rybczynski et al 2009), Enaliarctos is found in marine deposits, and is a flippered form resembling an otariid in general appearance (Berta 1991; Bebej 2009). While Enaliarctos is intermediate in morphology, sedimentological and biomechanical evidence suggests it was highly aquatic and fed in water like a modern pinniped (Berta 1991; Bebej 2009). Given that sexual size dimorphism is correlated with mating systems in modern pinnipeds (and other mammals), we can use morphological evidence to reconstruct the mating system of Enaliarctos and other extinct pinnipeds (Leutenegger and Kelly 1977; Cassini 1999; Playcan 2000). We describe a cranial specimen of Enaliarctos emlongi, report on new morphological evidence of sexual dimorphism in this taxon, and use 2D geometric morphometrics and phylogenetic comparative methods to characterize skullshape dimorphism in extant pinnipeds and Enaliarctos. We perform ancestral character estimation with and without Enaliarctos thereby allowing us to infer the mating system in the common ancestor of crown pinnipeds. Methods Comparative description and CT scanning. Following Rybczynski (2009), we use the stem definition of Pinnipedia, in order to include both the extant and fossil taxa (the latter occasionally referred to as pinnipedimorphs). High Resolution Computed Tomography T. M. Cullen et al. !6 scans of the small skull specimen of Enaliarctos emlongi (USNM 314290) were performed in order to examine the middle ear morphology (as the surface of the tympanic bulla had been previously removed from the holotype of E. emlongi, as well as in most other USNM Enaliarctos specimens in which the bullae are preserve, for examination