Sexual weapons are used in physical combat to secure mating opportunities; victorious males typically have larger body size and larger sexual weapons as a direct result of intrasexual selection (Geist 1999; Emlen 2008; McCullough et al. 2016; Sol et al. 2020). Structures that serve as intrasexual signals and weapons (e.g., ungulate antlers and horns) typically exhibit positive allometry in both developmental growth and evolution: As individuals grow and species evolve larger body sizes, they grow and evolve disproportionately larger ornaments than smaller individuals and species (Gould 1974; McCullough et al. 2015; Rico-Guevara and Hurme 2018; Somjee et al. 2021). Larger, stronger individuals invest more energy into these presumably honest signals of strength in order to avoid costly or injurious fights (Barrette 1977; Emlen 2008). Pure sexual weapons (e.g., tusks, claws, rhinoceros beetle horns), however, have evolved to provide advantages during intrasexual fights, are only used in combat, and thus provide little signaling value (McCullough et al. 2016; Rico-Guevara and Hurme 2018; Sol et al. 2020). Few studies, though, have examined static allometric growth or allometric evolution of these pure, non-signaling, sexual weapons, and even fewer examine these allometric relationships in species with multiple sexual weapons. In this study, we investigate the allometric relationships that influence the growth and evolution of tusks and antlers as sexual weapons within and among the artiodactyl families Tragulidae, Moschidae, and Cervidae, and among the Muntiacinae, the only ungulate group with both sexual weapons.
Sexual weaponry is a result of intrasexual selection (Emlen 2008), and weapons can vary in size, shape, and purpose across several classes of animals (McCullough et al. 2016). Sexual ornaments range between pure sexual weapons (e.g. beetle horns and mandibles) to pure sexual signals (e.g. eye stalks in flies). Weapons that fall in the middle of this continuum, such as ungulate antlers and fiddler crab claws, can serve both functions (McCullough et al. 2016). Beetle horns, for example, increase with body size and usually become the stronger strategy for attaining mates through physical combat rather than other non-combat sexual mating strategies (Moczek and Emlen 2000; McCullough et al. 2015). Some sexual weapons, though, can serve dual functions, as they are very often used as visual signals of dominance (McCullough et al. 2016; Rico-Guevara and Hurme 2018) and/or fighting ability (Mills et al. 2016) to other males. The large complex antler racks of male deer, for example, are critical fighting weapons of combat, are honest signals of their bearer’s strength and size, and may be used in female assessment of males (Vanpe et al. 2007). While antlers (and horns in bovids) are the more common sexual weapon among artiodactyls, tusks are the sole weapon in several groups and grow along with antlers in the Muntiacinae (muntjaks and tufted deer). This presence of dual weaponry in ungulates provides an opportunity to understand how selection may prioritize growth and maintenance of one weapon over the other and whether there are constraints on the size of such structures.
Possession of tusk-like canine teeth is the ancestral state for all Artiodactyls, with antlers, horns, and pronghorns evolving later in the cervids, bovids, and antilocaprids, respectively (Cabrera & Stankowich, 2018). Tusks were retained in the mouse deer and chevrotains (Tragulidae: three genera Moschiola, Hyemoschus, and Tragulus; Wilson and Mittermeier 2011), which are nocturnal and live in dense forests (Prothero 2007). Adult males use their large upper canines to attack in a sideways slashing motion targeting the neck and head of their opponent (Matsubayashi et al. 2003); these fights are likely often fatal (Prothero 2007). As ungulates evolved larger body sizes and moved into more open habitats, large tusks were lost with the evolution of antlers, horns, and pronghorns, but were re-evolved as the sole combat weapon in the Chinese water deer (Cervidae: Hydropotes; Fig. 1C) and musk deer (Moschidae: Moschus; Fig. 1D), both of which lack antlers but possess very large upper canines that reach 10 cm in length (Aitchison 1946; Fennessy 1984; Cabrera and Stankowich 2018).Living a “slinker” lifestyle in closed, forested environments favors the evolution of smaller “duiker”-like bodies for easier maneuverability (Geist 1999; Cabrera and Stankowich 2018), makes close-range combat essential for territory maintenance (Wilson and Mittermeier 2011), and favors the evolution and retention of tusks as the primary combat weapon in Artiodactyls (Cabrera and Stankowich 2018), where larger tusked males hold the best territories (Cooke, 2019). This lifestyle also likely results in minimal sexual selective pressure favoring an additional visual signal of dominance (i.e., antlers; Cabrera & Stankowich 2018). Open grassland habitats, on the other hand, favor visual displays of dominance rather than physical combat, which should result in larger ornamental weapons like antlers and horns and shorter tusks, which are limited in their ability to signal dominance from longer distances (Emlen 2008).
Within the cervids, the Muntiacinae (Muntiacus (Fig. 1A) and Elaphodus (Fig. 1B)) are very primitive deer that possess both tusks and antlers, and their antlers may have evolved in parallel with other cervids rather than being shared by their common ancestor (Groves and Grubb 1990). Males use large 2–4 cm upper canines, which begin emerging as early as five months and reach their maximum length around year five (Cooke, 2019), in physical combat to maintain control of access to mates (Fennessy 1984; Geist 1999). Tusks. In muntjaks, tusks are their main weapon; thus, damage to them can result in loss of territory and reduced mating opportunities (Cooke 2019). Elaphodus have the smallest antlers of all deer; they do not shed annually, and are so small that they can only be seen by parting the long tufts of hair on the pedicles (Fennessy 1984; Groves and Grubb 1990). Muntjacs have very long, permanent antler pedicels with short deciduous antlers (Fig. 1A; Fig. 2B; Cooke 2019). Muntjacs perform a “dominance display” before potential fights to deter the weaker opponent from engagement, which results in a reduction in frequency of fights (Barrette 1977) similar to other antlered deer. Because the Muntiacinae possess both versions of combat weaponry, they provide an opportunity to compare the allometric developmental and evolutionary relationships for species with two distinct types of sexual weapons: one pure weapon (tusks) and one signal/weapon (antlers).
The allometric relationships (static and evolutionary) between sexual ornaments/weapons and body size have been studied for several types of weapons in different taxa. Previously, it was assumed that most sexually selected traits scale positiviely allometrically with body size (Kodric-Brown et al. 2006; O'Brien et al. 2018), and there are plenty studies that support positive static allometric relationships between sexually selected traits and body size (Simmons and Tomkins 1996; Kodric-Brown et al. 2006; Ñoñiguez et al. 2019; Graham et al. 2020; Powell et al. 2020). Evolutionarily, however, there has been recent support that positive allometry, while common, is not a universal rule in sexually selected traits (Bonduriansky and Day 2003; Pomfret and Knell 2006; Eberhard et al. 2018; O'Brien et al. 2018; Somjee et al. 2021). For example, Bonduriansky (2007) summarized that some weapons and ornaments can scale isometrically or negatively allometrically, and O’Brien and colleagues (2018) suggested that the positive allometry hypothesis for sexually selected traits should only be applied to visual signals of body size or quality and be tested against a reference trait without signaling function. Cranial weapons in bovids, cervids, and beetle species, indeed, have a positively allometric relationship with body mass in smaller species, but it levels off in larger species (i.e., weapons stop increasing in length with body mass in larger species), suggesting that there are physical constraints on growing and maintaining bigger weapons at very large body masses (Emlen 1996; Lemaitre et al. 2009; McCullough et al. 2015; Romiti et al. 2015; Tidière et al. 2017; Chen et al. 2020). Although, recent evidence suggests that, intraspecifically, continued positively allometrically scaling weapons at extreme sizes may be possible through lower metabolic rates (Somjee et al. 2021). Gould (1974) found that the massive extinct Irish Elk (Megaloceros giganteus) violates this physical constraint explanation in cervids as their antlers are on the same positively allometric trajectory as smaller cervids. Whereas the equally large moose (Alces spp) fall well below this trajectory and likely drive the appearance of physical constraints on larger antlers in large extant cervids (Gould 1974). Tusks have evolved independently across multiple mammalian taxa (e.g., whales, elephants, ungulates), but their static and evolutionary allometric growth patterns are not well understood. Tusk girth, weight, and length in male narwhals (Monodon monoceros) all had positively allometric relationships with body length (Gerson and Hickie 2011). It is unknown how the presence of both a pure weapon and a weapon/ornament in the same species will alter allometric relationships.
Here, we analyze the relationship between overall body size (shoulder height, body mass, and skull length) and sexual weaponry among only tusked, both tusked and antlered, and only antlered ungulates. In our static allometry tests, we hypothesized that the growth of larger body sizes favors the growth of disproportionately longer antlers and longer tusks when they are the sole sexual weapon available (i.e., positively allometric), however tusks are not generally visual signals of size (i.e., pure weapons) and may not scale positively allometrically. When both types of weapons are present, however, we hypothesized that larger body sizes favor disproportionately larger antlers but not tusks as larger antlers make for stronger signals and may be advantageous in fights. Evolutionarily, we hypothesized that evolving larger body sizes favors disproportionately larger weapons, regardless of whether one or two types of weapons are present, but that dual-weapon species may invest less in each weapon relative to single-weapon species of similar size. We examined these relationships both within several species of tusked adult ungulates, and between species of tusked and antlered deer using linear regression and phylogenetic generalized least squares (PGLS) analyses respectively.