Living in mixed-sex groups limits sexual selection in coloration and pelage appendages in bovids

Among mammals, bovids provide some of the most striking examples of sexual dimorphism in colouration and pelage appendages, such as beards and manes. This dimorphism is usually assumed to have evolved through sexual selection on males in the context of intra- or intersexual communication. However, the sexes look similar in several bovid species thought to be characterized by large opportunities for sexual selection, hinting at fitness costs of dimorphic traits due to other selection pressures. This study applies the comparative method with phylogenetic control to identify the factors promoting and constraining the evolution of dimorphism in colouration and pelage appendages across bovids. We found that trait dimorphism correlated positively with large breeding group size, an indicator of the intensity of sexual selection, and negatively with male territoriality, which is also likely to affect the operation of sexual selection. The relative rarity of colour and pelage dimorphism in species with territorial mating systems may be explained by weaker sexual selection due to difficulty in monopolizing females and/or sexual selection targeting other traits, such as territorial quality as an extended phenotype. We also found that colour and pelage dimorphism were reduced in species spending more time in mixed-sex groups outside the breeding season, possibly due to increased predation costs from non-uniformity This suggests that benefits from integration into mixed-sex groups select against the extravagant male morphologies otherwise promoted by sexual selection.

Methods
Data on colouration sexual dimorphism (CSD) and pelage appendage sexual dimorphism (PASD) were collected for 110 species in the family Bovidae. The scores for CSD and PASD were obtained by visual scoring of images from males and females of each species (range 2-8 pictures per species) obtained from: www.arkive.com; www.encyclopediaoflife.com; www.ultimateungulate.com; Costello JR. (2016). Bovids of the world. Princeton (USA): Princeton University Press. All pictures referred to the same subspecies. 

CSD was scored on eight distinct body regions: (i) head; (ii) neck; (iii) flank, shoulder, humerus; (iv) rump, femur; (v) upper front leg; (vi) lower front leg; (vii) upper hind leg; and (viii) lower hind leg. CSD for each body region was scored according to a three-point scale: 0 - no difference; 1 - the difference in background colour or contrast markings (i.e. presence in one sex only); 2 - the difference in both background colour and contrast markings. Background hair colour was compared to a reference of five colour categories: (i) white (de-pigmented); (ii) phaeomelanin - yellow/red; (iii) eumelanin - brown; (iv) eumelanin – grey; and (v) eumelanin - black. The background colour was scored as dimorphic if the same body region was assigned to different categories in males and females. The overall CSD index presented in this dataset was calculated as the sum of the scores for all eight body regions.

PASD was scored on inter-sexual differences in (i) frontal hair tuft; (ii) beard or ventral mane; (iii) dorsal mane; (iv) cape (covering both dorsal and ventral parts of the neck); (v) front leg pantaloons; and (vi) hind leg pantaloons. A four-point visual scale was used: 0 - no difference in the pelage appendage between the sexes; 1 – the appendage differs in either size or colour between the sexes; 2 – the appendage differs in both size and colour between the sexes; 3 – the appendage is present in one sex only. The overall PASD index presented in this dataset was calculated as the sum of scores for all the pelage appendages in each species.

Sexual aggregation in this dataset was defined as the tendency for males and females to form mixed-sex herds outside of the breeding context, and scored on a three-point scale: 1 – never forming mixed-sex groups with multiple males (including species in which males are solitary or live in segregated, unisexual groups, only joining female groups in search of mating opportunities); 2 - sometimes forming multi-male mixed-sex groups (including species in which only some males are found in multimale mixed-sex groups, either because not all males join these groups or because associations are temporary, e.g. during migrations); and 3 - generally forming multi-male mixed-sex groups (including species in which the sexes typically aggregate, although some males may temporarily join bachelor groups). The scoring was based on available published material listed in the Supplementary Material to the manuscript.

Habitat openness was scored based on the probability of detecting large mammals in each of the nine different IUCN habitat categories (www.iucnredlist.org): tropical forest (0.1), temperate forest (0.2), wetland (0.3), tropical shrubland (0.5), temperate shrubland (0.6), savannah (0.7), grassland (0.8); rocky areas (0.8), and desert (0.95). The species-specific score for habitat openness was calculated as the mean detection probability across all habitat categories occupied by the species.

Data for average breeding group size (Group Size) and male mating strategy (Male Mating Strategy) were derived from published literature reported in the Supplementary Material to the manuscript. Male mating strategy was defined as T (territorial) or NT (non-territorial).