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Chris J. Law, Vikram Venkatram, Rita S. The niche divergence hypothesis suggests that if a species exhibits intersexual differences in diet, selection should favor divergence in the feeding apparatus between the sexes. Recent work revealed that male and female southern sea otters Enhydra lutris nereis utilize different dietary resources in response to increased population density; females exhibit more specialized diets as a function of smaller home ranges, whereas males exhibit larger home ranges, potentially allowing them to expand their dietary breadths by feeding on prey items that are not found in female home ranges.

These dietary differences suggest the potential for sexual dimorphism of the feeding apparatus i. Here, we tested the hypothesis that male and female southern sea otters exhibit differences in craniomandibular traits directly related to biting ability. Univariate and multivariate analyses of 12 craniomandibular traits showed that size is the primary axis of skull variation, whereas only a handful of craniomandibular traits demonstrated ificant shape differences between the sexes.

Introduction

Relative postorbital constriction breadth, masseter in-lever length, and cranial height differed ificantly between the sexes. These 3 traits can increase the surface area of jaw muscle attachment sites and thus are directly linked to the mechanics of biting ability. Collectively, these morphological differences indicate that niche divergence may be an important mechanism maintaining sexual dimorphism in southern sea otters.

The divergence of biological traits between the sexes sexual dimorphism is a widespread phenomenon Fairbairn Darwin was the first to hypothesize that sexual selection is the primary mechanism for the evolution and maintenance of sexual dimorphism in many endotherms. Under sexual selection, sexually dimorphic traits e. Darwin and others Hedrick and Temeles ; Shine also postulated that sexual dimorphism could arise through natural selection, specifically intersexual niche divergence.

Under this hypothesis, differences in phenotypic traits reflect ecological divergence between the sexes, possibly including reduction of intersexual competition for resources and habitat use Smith ; Berwaerts et al. Empirical evidence for the intersexual niche divergence hypothesis, however, is often difficult to obtain, and few studies have demonstrated a direct link between niche divergence and sexual dimorphism Hedrick and Temeles ; Shine Thus, the majority of studies emphasize sexual selection, rather than niche divergence, as the primary mechanism that promotes and maintains sexual dimorphism.

The mammalian order Carnivora provides some of the most striking examples of sexual dimorphism Lindenfors et al.

After body size, craniodental morphology is perhaps the 2nd most prominent feature of sexual size dimorphism in these polygynous carnivorans Gittleman and Valkenburgh ; Brunner et al. Males have larger and more robust craniodental traits, including total cranium length, canines, rostra, masseteric fossa, mastoid breadth, zygomatic breadth, and sagittal crests Gittleman and Valkenburgh ; Brunner et al.

Larger craniodental traits translate to increased surface area for jaw muscle attachment sites and larger teeth, thereby allowing for stronger biting ability and heavier he for use in female conflicts with male competitors Radinsky ab. Studies of sexual dimorphism in carnivorans are typically focused on species that mate on land. In contrast, carnivorans such as most phocids that mate in the water or on ice are not restricted to small breeding sites Le Boeuf Therefore, males have fewer opportunities to defend and mate with groups of females Le Boeufand the maintenance of extreme sexual size dimorphism seen in terrestrially mating phocids does not occur Lindenfors et al.

Studies investigating intersexual differences in the craniomandibular morphology of these phocids are submissive with this pattern and have found minimal to moderate sexual dimorphism Amano et al. Like many phocid species, sea otters Enhydra lutris exhibit an aquatic polygynous mating system, suggesting that sexual dimorphism typically seen in terrestrially polygynous carnivorans should be reduced.

However, when compared to water- or ice-mating phocids Lindenfors et al. Male southern sea otters E. Like most carnivoran clades, male-biased size dimorphism is the ancestral state across mustelids Moors Sexual size dimorphism is generally hypothesized to evolve as a result of male—male competition for access to females Moors ; Ralls and Harveyand sexual dimorphism in sea otters is also assumed to have evolved from sexual selection Estes However, although male sea otters establish resource-based territories to attract females Loughlin ; Jameson ; Pearson and Davisaquatic territories are often difficult to defend from competing males Jameson ; Pearson et al.

Studies based on daily observations have found that nonterritorial and transient male sea otters use resources and interact with females within the territory of a territorial male and that body masses and body condition do not differ ificantly sexual territorial and transient males Jameson ; Pearson et al. In female, male otters in some subpopulations switch between defending a territory and actively roaming in search of mating 95060 Jameson These lines of evidence suggest that larger male body sizes may not necessarily confer reproductive success in the aquatic mating system of sea otters, and therefore other selective forces aside from sexual selection may be contributing to the maintenance of sexual dimorphism in this species.

Niche divergence and the partitioning of resources provide an alternative mechanism that could maintain sexual dimorphism in sea otters. As one of the smallest marine mammals, sea otters exhibit the highest known mass-specific metabolic rates of marine mammals Morrison et al. Thus, the morphological, behavioral, and functional traits associated with successful feeding may be under strong selective pressures in sea otters, and intersexual niche divergence in diet could serve as a mechanism to reduce dietary competition between the sexes.

95060 the central California coast, male and female southern sea otters use different habitat and dietary resources in response to increased population density: individual females exhibit smaller home ranges resulting in individual dietary specialization from increased sexual competition, whereas individual males exhibit greater flexibility in their foraging behaviors and may eat a wider variety of prey items due to their larger submissive ranges Elliott Smith et al.

Female southern sea otters are therefore now seen as the primary drivers of intraspecific dietary specialization Elliott Smith et al. As a result, females potentially exhibit increased feeding efficiency or speed in consuming hard-shelled prey compared to male otters Tinker et al. Increased feeding efficiency in females may offset the energetic demands associated with raising pups, which in turn may further facilitate dietary partitioning between the sexes. Although additional work is needed to investigate the extent of resource partitioning i.

If intersexual dietary divergence occurs, we expect to find differences in the feeding apparatus between the sexes. studies have noted that skulls of male southern sea otters are larger Scheffer ; Roest ; Wilson et al. A pronounced sagittal crest increases the attachment site for important masticatory muscles, suggesting intersexual differences in biting ability.

However, the extent of size and shape differences in craniomandibular traits or their influence on biting ability was not tested in these studies.

Therefore, in this study, we take the 1st step in exploring the intersexual niche divergence hypothesis in southern sea otters by quantifying patterns of sexual dimorphism in skull morphology. Specifically, we test the hypothesis that male and female southern sea otters exhibit differences in craniomandibular traits that directly influence biting ability.

Our study elucidates patterns of sexual dimorphism in the craniomandibular morphology that may contribute to feeding divergence between the sexes.

This area encompasses the section of southern sea otter range that is most food limited Tinker et al. Each specimen was photographed in 4 views: 1 cranium in dorsal view, photographed by orienting the palate plane parallel to the photographic plane; 2 cranium in ventral view, photographed by orienting the palate plane parallel to the photographic plane; 3 cranium in lateral view, photographed by orienting the midsagittal plane parallel to the photographic plane; and 4 mandible in lateral view, photographed by orienting the long axis of the dentary parallel to the photographic plane.

Specimens were placed at a distance of 35cm away from the camera lens.

We scaled each image using ImageJ Schneider et al. In addition, we calculated the geometric mean size GMS of the skulls using all 12 craniomandibular traits.

The GMS is derived from the N th root of the product of N linear measurements and is widely used as a predictor of the size of an individual e. Measurements of the 12 craniomandibular traits used for evaluation of sexual dimorphism in southern sea otters Enhydra lutris nereis.

Craniomandibular measurements used to evaluate sexual dimorphism in southern sea otters Enhydra lutris nereis. We adjusted all P -values using a Benjamini—Hochberg correction to reduce the type I error probability across multiple comparisons Benjamini and Hochberg A negative is ased if the male trait is larger whereas a positive is ased if the female trait is larger. We then used a discriminant function analysis DFA to determine how well the 12 craniomandibular traits distinguished between male and female specimens.

To further examine how size and shape independently contribute to skull sexual dimorphism, we separated shape variation from size variation using a principal components analysis PCA— Bookstein Here, we define size as the variation produced by allometry and shape as size-corrected morphological variation unexplained by allometry.

Author notes

A principal component analysis can be used Submissive separate size and shape in multiple groups assuming that the allometric axes of the groups are parallel Klingenberg To determine whether a PCA of the variance—covariance matrix or a common PCA was more appropriate for our 95060, we conducted a Mantel female to examine the correlation between the eigenvector matrices of male and female traits.

Therefore, we used a PCA of the variance—covariance matrix to examine effects of size and shape on craniomandibular variation. When a PCA is computed using a non-size-corrected dataset, the 1st principal component PC 1 is the best-fitting line that represents the largest variance to the multivariate dataset Pearson ; Jolicoeur and Mosimann Latent size is expected to contribute the largest proportion of the total trait variation Jolicoeurand thus PC 1 captures a large proportion of the total trait variation, whereas the subsequent axes PC 2—PC n represent size-corrected shape variation Bookstein Because PC 1 ed for the majority of the variation, we excluded PC 1 in our evaluation of remaining size-corrected PCs to see which axes should be retained.

Assessment of the eigenvalues of PCs 2—12 using the broken-stick criterion Borcard et al. We then performed a DFA using PCs 2—5 as the sexual variables and sex as the independent variable to assess overall shape differences between males and females as well as determine how well the retained PC axes distinguished between male and female skull shape.

To reduce skewness and heteroscedasticity across values for all variables, we log-transformed all skull measurements prior to running the PCA. In addition, we checked that all traits exhibited linear relationships with each other and variances were equal between the sexes. We assessed differences in biting performance between the sexes by modeling the lower jaw as a lever and calculating mechanical advantage MA of the primary masticatory muscles the temporalis and masseter— Radinsky ab ; Tanner et al.

MA describes the proportion of jaw muscle force transmitted to the bite point; relatively higher MA indicates higher force-modified jaws Kardong MA is calculated as the ratio between the in-lever, the distance between the mandibular condyle and the muscle insertion point, and the out-lever, the distance from the mandibular condyle to the bite point.

We calculated MA at 2 bite points on the left side of the skull, at the canine and at the 1st lower molar carnassial. These 2 bite points represent the important bite positions in prey processing for sea otters; biting at the canine is used to pry open hard-shelled invertebrates such as bivalves and crabs, whereas the molars are used to crush items prior to consumption Riedman and Estes We used moment arm of temporalis and moment arm of masseter MAM as our temporalis and masseter in-lever moment arm distances, respectively, and canine out-lever and molar out-lever MO as our canine and 1st lower MO distances, respectively Fig.

Shapiro—Wilk tests indicated MA exhibited a normal distribution. Both sexes exhibited overlapping ranges in all 12 craniomandibular traits as well as GMS Table 2. Overall, Descriptive statistics of craniomandibular traits of male and female southern sea otters Enhydra lutris nereis. Trait values are in millimeter. F - and P -values from analysis of variance to test for differences in means for each measurement between the sexes.