Variation in guenon skulls (I): species divergence, ecological and genetic differences

Guenons are the most diverse clade of African monkeys. They have varied ecologies, include arboreal and terrestrial species, and can be found in nearly every region of sub-Saharan Africa. Species boundaries are often uncertain, with a variable number of species and subspecies mostly recognised on the basis of their geographic distribution and pelage. If guenon soft tissue patterns show high variability, the same does not seem to hold for skull morphology. Guenon skulls are traditionally considered relatively undifferentiated and homogeneous. However, patterns of variation in skulls have never been examined using a large number of specimens sampled across the breadth of species diversity. Thus, in the present study, skulls of adult guenons and two outgroup species are analysed using three-dimensional geometric morphometrics. Three-dimensional coordinates of 86 anatomical landmarks were measured on 1,315 adult specimens belonging to all living guenon species except Cercopithecus dryas. Species are well-discriminated using shape but the best discrimination occurs when species have either a long evolutionary history (e.g., Allenopithecus nigroviridis) or represent extremes of size variation (Miopithecus sp. and Erythrocebus patas). Interspecific phenetic relationships reflect size differences. Four main clusters are found that mainly correspond to four size groups: the smallest species (Miopithecus sp.), the largest species (E. patas plus the study outgroups), a group of medium-small arboreal guenons, and a group of medium-large arboreal and terrestrial guenons. Correlations between interspecific shape distances and interspecific differences in size are higher than between shape distances and genetic distances. However, if only the component of interspecific shape variation which is not correlated to evolutionary allometry is used in the comparison with genetic distances, correlations are up to 1.4 times larger than those including allometric shape. The smallest correlations are those between shape and ecological distances, which is consistent with the lack of clusters clearly reflecting broad ecological specialisations (e.g., arboreality versus terrestriality). Thus, size, which is generally considered more evolutionarily labile than shape, seems to have played a major role in the evolution of the guenons. The incongruence between interspecific shape differences and phylogeny might be explained by a large proportion of shape changes having occurred along allometric trajectories that tend to be conserved within this clade.     

Sexual dimorphism,mating system,and effect of phylogeny in De Brazza's monkey (Cercopithecus neglectus)

De Brazza's monkey (Cercopithecus neglectus), like other guenons, shows marked sexual dimorphism in an array of features. While strong sexual dimorphism is generally associated with a polygynous mating system, populations of De Brazza's monkeys in Gabon are reportedly monogamous. An explanation of this unique phenomenon is offered here. Patterns of sexual dimorphism are examined for morphology, growth and development, behavior, and ecology, and field and captive studies on the social organization and mating system of De Brazza's monkey and congeneric guenon species are reviewed. Based on the findings, it is postulated that 1) De Brazza's monkeys are not strictly monogamous, but exhibit interpopulational variation in their mating system, from facultative monogamy to mild polygyny; 2) marked sexual dimorphism most likely reflects the effect of the historical-phylogenetic factor; ie, it represents a holdover of a degree of dimorphism established earlier in evolutionary history when the degree of polygyny Was higher; and 3) lessening in the degree of polygyny and a tendency toward monogamy represents a consequence of selection toward small group size. Small group size, a unique antipredator strategy, and failure to form polyspecific associations are ultimately most likely the result of intragroup and interspecific competition and predation pressure.     

Sexual dimorphism in the canines and skulls of carnivores: effects of size, phylogency, and behavioural ecology

Sexual dimorphism in craniodental features is investigated in a sample of 45 carnivore species in relation to allometry, phylogeny, and behavioural ecology. Dimorphism is more pronounced in both upper and lower canine size and strength than in carnassial size, skull dimensions and biomechanical features, but all dimorphism indices covary. As with most morphological characters, differences in canine sexual dimorphism are significantly related to phylogeny, estimated from either taxonomic rankings or a limited matrix of molecular distances; in particular, mustelids, felids and procyonids are more dimorphic than other carnivore families. Thus, because of problems related to species dependence in comparative data, remaining analyses are based on phylogenetically transformed values using a spatial autoregressive method.
In contrast to other mammals, sexual dimorphism in carnivore canines is not correlated with differences in body weight, skull length or basicranial axis length. Nor is it correlated with categorical variables of activity pattern, habitat, or diet. In our Carnivore sample, canine dimorphism is related only to breeding system: uni-male, group-living (harem) species have significantly greater canine dimorphism than multi-male, multi-female groups and monogamous pair-bonding species. By contrast, dimorphism in carnassial size is related to dietary differences, specifically greater dimorphism in meat-eating species, and not breeding patterns. Dimorphism in estimates of jaw muscle size suggest functional demands from both diet and breeding type. It is concluded that, befitting patterns of heterodont dentition, sexual selection influences variation in canine dimorphism while feeding ecology is related to carnassial dimorphism.     

Sexual dimorphism in bill morphology and feeding ecology in Cory's shearwater (Calonectris diomedea)

The bill is a sexually dimorphic structure in many bird species and implicated in numerous functions. Sexual differences may arise from sexual selection or ecological divergence. Here, we examined differences in bill size and shape between males and females and explored to what extent these relate to feeding ecology of each sex in Cory's shearwater (Calonectris diomedea). We applied linear measurements and geometric morphometric methods to examine sexual differences in bill size and shape. We investigated feeding ecology by tracking foraging movements during the breeding period and by analysing stable isotope signatures in blood during the breeding period and in feathers grown during the non-breeding period. Bill traits were all sexually dimorphic, both in absolute and relative terms, and scaled hypermetrically with body mass in several characters in males. However, males and females did not differ in their feeding areas or isotopic signatures and no significant correlation was observed between these traits and bill dimorphism. Therefore, we discard the foraging-niche divergence hypothesis, and suggest that sexual dimorphism in bill size in this species is more likely driven by sexual selection related to antagonistic interactions.     

Sexual dimorphism in the skull geometry of newt species of <Emphasis Type="Italic">Ichthyosaura,Triturus</Emphasis> and <Emphasis Type="Italic">Lissotriton</Emphasis> (Salamandridae,Caudata, Amphibia)

In this study, we applied geometric morphometrics to explore variations in the level and pattern of sexual size dimorphism (SSD) and sexual shape dimorphism (SShD) of the ventral cranium in three different Modern Eurasian newt taxa (Ichthyosaura alpestris, Triturus species group and Lissotriton vulgaris). The ventral cranium is the part of the skull that is more directly related to foraging and feeding. Our results indicate that the level and pattern of sexual dimorphism in the ventral cranium differ among Modern Eurasian newt taxa. Regarding sexual dimorphism in skull size, Ichthyosaura alpestris and Triturus species show female-biased patterns (females are larger than males), whereas Lissotriton vulgaris appears to be non-dimorphic in skull size. In I. alpestris and Triturus species, SShD is mostly absent, whereas in L. vulgaris, SShD is more pronounced. A high level of variation between populations in both SSD and SShD indicates that local conditions may have a profound effect on the magnitude and direction of sexual dimorphism. The significant sexual differences in ventral cranium size and shape indicate possible subtle intersexual differences in ecological demands due to diet specialisation, in spite of similar general ecological settings.     

An ontogenetic perspective on the study of sexual dimorphism, phylogenetic variability, and allometry of the skull of European ground squirrel, Spermophilus citellus (Linnaeus, 1766)

Most studies of morphological variability in or among species are performed on adult specimens. However, it has been proven that knowledge of the patterns of size and shape changes and their covariation during ontogeny is of great value for the understanding of the processes that produce morphological variation. In this study, we investigated the patterns of sexual dimorphism, phylogenetic variability, and ontogenetic allometry in the Spermophilus citellus with geometric morphometrics applied to cross-sectional ontogenetic data of 189 skulls from three populations (originating from Burgenland, Banat, and Dojran) belonging to two phylogenetic lineages (the Northern and Southern). Our results indicate that sexual dimorphism in the ventral cranium of S. citellus is expressed only in skull size and becomes apparent just before or after the first hibernation because of accelerated growth in juvenile males. Sexes had the same pattern of ontogenetic allometry. Populations from Banat and Dojran, belonging to different phylogroups, were the most different in size but had the most similar adult skull shape. Phylogenetic relations among populations, therefore, did not reflect skull morphology, which is probably under a significant influence of ecological factors. Populations had parallel allometric trajectories, indicating that alterations in development probably occur prenatally. The species’ allometric relations during cranial growth showed characteristic nonlinear trajectories in the two northern populations, with accelerated shape changes in juveniles and continued but almost isometric growth in adults. The adult cranial shape was reached before sexual maturity of both sexes and adult size after sexual maturity. The majority of shape changes during growth are probably correlated with the shift from a liquid to a solid diet and to a lesser degree due to allometric scaling, which explained only 20 % of total shape variation. As expected, viscerocranial components grew with positive and neurocranial with negative allometry.     

Variation in the digging apparatus of the subterranean silvery mole-rat, Heliophobius argenteocinereus (Rodentia, Bathyergidae): the role of ecology and geography

The skull of most subterranean tooth-digging rodents is markedly affected by their digging mode. In the present study, we investigated the cranial variation in a strictly subterranean, highly specialized Afrotropical tooth-digger, Heliophobius argenteocinereus (Bathyergidae, Rodentia), using a geometric morphometric approach and evaluated the effect of different factors on size and shape differences among four populations. No evidence for sexual dimorphism was found in skull size or shape. The cranial shape variation was large and influenced mainly by the type of habitat (miombo woodland versus farmland and grassland) and the latitudinal gradient. The dorsal side of the skull appears to be more plastic and adaptable to local environments, as well as more independent of size, than the ventral side. Only the shortening of the rostrum is presumably an adaptive process independent of size that leads to an increase of efficacy of the tooth-digging apparatus in Heliophobius , whereas the increase in the in-force and the more procumbent incisors both comprise size-related changes caused by ontogenetic allometric growth.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 822–831.     

Shape,size, and maturity trajectories of the human ilium

Morphological traits of the ilium have consistently been more successful for juvenile sex determination than have techniques applied to other skeletal elements, however relatively little is known about the ontogeny and maturation of size and shape dimorphism in the ilium. We use a geometric morphometric approach to quantitatively separate the ontogeny of size and shape of the ilium, and analyze interpopulation differences in the onset, rate and patterning of sexual dimorphism. We captured the shape of three traits for a total of 191 ilia from Lisbon (Portugal) and London (UK) samples of known age and sex (0–17 years). Our results indicate that a) there is a clear dissociation between the ontogeny of size and shape in males and females, b) the ontogeny of size and shape are each defined by non‐linear trajectories that differ between the sexes, c) there are interpopulation differences in ontogenetic shape trajectories, which point to population‐specific patterning in the attainment of sexual dimorphism, and d) the rate of shape maturation and size maturation is typically higher for females than males. Male and female shape differences in the ilium are brought about by trajectory divergence. Differences in size and shape maturation between the sexes suggest that maturity may confound our ability to discriminate between the sexes by introducing variation not accounted for in age‐based groupings. The accuracy of sex determination methods using the ilium may be improved by the use of different traits for particular age groups, to capture the ontogenetic development of shape in both sexes. Am J Phys Anthropol 156:19–34, 2015 © 2014 Wiley Periodicals, Inc.     

猕猴属种间颅骨差异的探讨

为了研究狒猴属的颅骨差异性,从面探讨种间在形态、功能和系统分化方面联系,测定了１１１个猕猴种类的７７个颅骨变量,用于主成分分析和判别分析。应用巢式分析方法,分析过程包括３个步骤。所有变量根据功能和部位的不同首先分为７个单位：下颌、下颌齿、上颌齿、上面颅、下面颅,、面颅后部和颅腔。第２步根据它们所揭示的相似性（具有相同的种间及种内差异性类型）合并为３个解剖区域：咀嚼器官（下颌、下颌齿、上颌齿）,面颅     

Intraspecific variation in the skull morphology of the black caiman Melanosuchus niger (Alligatoridae,Caimaninae)

Melanosuchus niger is a caimanine alligatorid widely distributed in the northern region of South America. This species has been the focus of several ecological, genetic and morphological studies. However, morphological studies have generally been limited to examination of interspecific variation among extant species of South American crocodylians. Here, we present the first study of intraspecific variation in the skull of M. niger using a two‐dimensional geometric morphometric approach. The crania of 52 sexed individuals varying in size were analysed to quantify shape variation and to assign observed shape changes to different types of intraspecific variation, that is, ontogenetic variation and sexual dimorphism. Most of the variation in this species is ontogenetic variation in snout length, skull depth, orbit size and the width of the postorbital region. These changes are correlated with bite force performance and probably dietary changes. However, a comparison with previous functional studies reveals that functional adaptations during ontogeny seem to be primarily restricted to the postrostral region, whereas rostral shape changes are more related to dietary shifts. Furthermore, the skulls of M. niger exhibit a sexual dimorphism, which is primarily size‐related. The presence of non‐size‐related sexual dimorphism has to be tested in future examinations.     

Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions

Adaptive divergence of phenotypes, such as sexual dimorphism or adaptive speciation, can result from disruptive selection via competition for limited resources. Theory indicates that speciation and sexual dimorphism can result from identical ecological conditions, but co-occurrence is unlikely because whichever evolves first should dissipate the disruptive selection necessary to drive evolution of the other. Here, we consider ecological conditions in which disruptive selection can act along multiple ecological axes. Speciation in lake populations of threespine sticklebacks (Gasterosteus aculeatus) has been attributed to disruptive selection due to competition for resources. Head shape in sticklebacks is thought to reflect adaptation to different resource acquisition strategies. We measure sexual dimorphism and species variation in head shape and body size in stickleback populations in two lakes in British Columbia, Canada. We find that sexual dimorphism in head shape is greater than interspecific differences. Using a numerical simulation model that contains two axes of ecological variation, we show that speciation and sexual dimorphism can readily co-occur when the effects of loci underlying sexually dimorphic traits are orthogonal to those underlying sexually selected traits.     

Sexual dimorphism of skull shape in a lacertid lizard species (Podarcis spp., Dalmatolacerta sp., Dinarolacerta sp.) revealed by geometric morphometrics

Geometric morphometric techniques were used to examine allometric and non-allometric influences on sexual shape dimorphism (SShD) in the ventral cranium (skull base, palate and upper jaw) of four species of lacertid lizards (Podarcis muralis, Podarcis melisellensis, Dalmatolacerta oxycephala, Dinarolacerta mosorensis). These species differ in body shape, ecology and degree of phylogenetic relatedness. The structures of the ventral cranium that were studied are directly involved in the mechanics of feeding and are connected to the jaw musculature; these structures are potentially subject to both sexual and natural selection. Allometry accounted for a considerable degree of cranial shape variation between the sexes. Allometric shape changes between individuals with smaller cranium size and individuals with larger cranium size are mostly related to changes in the skull base showing pronounced negative allometry. The rostral part, however, either scaled isometrically or showed less pronounced negative allometry than the skull base. Non-allometric intersexual shape variation predominantly involved changes related to the jaw adductor muscle chamber, i.e., changes that are associated with biomechanically relevant traits of the jaw system in females and males. Both allometric and non-allometric shape changes appeared to be species-specific. Our results indicate that natural and sexual selection may be involved in the evolution of SShD.     

Human fertility variation, size-related obstetrical performance and the evolution of sexual stature dimorphism

In several animal species, change in sexual size dimorphism is a correlated response to selection on fecundity. In humans, different hypotheses have been proposed to explain the variation of sexual dimorphism in stature, but no consensus has yet emerged. In this paper, we evaluate from a theoretical and an empirical point of view the hypothesis that the extent of sexual dimorphism in human populations results from the interaction between fertility and size-related obstetric complications. We first developed an optimal evolutionary model based on extensive simulations and then we performed a comparative analysis for a total set of 38 countries worldwide. Our optimization modelling shows that size-related mortality factors do indeed have the potential to affect the extent of sexual stature dimorphism. Comparative analysis using generalized linear modelling supports the idea that maternal death caused by deliveries and complications of pregnancy (a variable known to be size related) could be a key determinant explaining variation in sexual stature dimorphism across populations. We discuss our results in relation to other hypotheses on the evolution of sexual stature dimorphism in humans.     

Geographic variation in size and sexual dimorphism of North American weasels

Geographic variation in size (skull length) and sexual dimorphism in Mustela erminea, Mustela frenata and Mustela nivalis in North America is described and analysed in relation to latitude, longitude, climatic variables, and sympatry or allopatry of these species. Only erminea increases in size with latitude; it does so regardless of the presence or absence of frenata or nivalis. Latitude is a better predictor of size in erminea than available measures of climate, seasonality or prey size. There is no evidence for character displacement between any pair of species. The sexes covary in size in frenata and erminea , and probably in nivalis , although geographic variation in sexual dimorphism occurs in frenata and erminea. The principal cause of sexual dimorphism appears to be sexual selection for large size in males rather than the high energetic requirements resulting from an elongate body shape. However, prey size may constrain female size (and possibly also male size). Regional differences in the abundance of prey during the growth of young weasels may affect adult size much more in males than in females and contribute to geographic variation in sexual dimorphism.     

Sexual dimorphism of head morphology in three‐spined stickleback Gasterosteus aculeatus

This study examined sexual dimorphism of head morphology in the ecologically diverse three‐spined stickleback Gasterosteus aculeatus. Male G. aculeatus had longer heads than female G. aculeatus in all 10 anadromous, stream and lake populations examined, and head length growth rates were significantly higher in males in half of the populations sampled, indicating that differences in head size increased with body size in many populations. Despite consistently larger heads in males, there was significant variation in size‐adjusted head length among populations, suggesting that the relationship between head length and body length was flexible. Inter‐population differences in head length were correlated between sexes, thus population‐level factors influenced head length in both sexes despite the sexual dimorphism present. Head shape variation between lake and anadromous populations was greater than that between sexes. The common divergence in head shape between sexes across populations was about twice as important as the sexual dimorphism unique to each population. Finally, much of the sexual dimorphism in head length was due to divergence in the anterior region of the head, where the primary trophic structures were found. It is unclear whether the sexual dimorphism was due to natural selection for niche divergence between sexes or sexual selection. This study improves knowledge of the magnitude, growth rate divergence, inter‐population variation and location of sexual dimorphism in G. aculeatus head morphology.     

Patterns of cranial sexual dimorphism in certain groups of extant hominoids

This paper presents a study of patterns of cranial variation within and between extant hominoids. Particular attention is paid to the relationship between sexual dimorphisms and size differences between sexes. It emerges that shape contrasts between sexes are closely linked to size differences whilst variance dimorphism appears to be relatively independent of size effects. This study demonstrates that there are differences between the hominoids in their magnitudes and patterns of sexual shape contrasts. These types of differences are also found to exist between subgroups of modern humans. It is suggested that the differences which occur between hominoid groups in their patterns of sexual dimorphism are probably the result of a mixture of time and rate hypermorphoses (in males relative to females) acting upon different ontogenetic trajectories. The findings of this study suggest the need for caution in extrapolating from the sexual dimorphisms found in living hominoids to hypothesized dimorphisms in fossils.     

Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics

Podarcis bocagei and Podarcis carbonelli are two lacertid species endemic to the western Iberian Peninsula, and both show head size and shape sexual dimorphism. We studied immature and adult head sexual dimorphism and analysed ontogenetic trajectories of head traits with body and head size, aiming to shed light on the proximate mechanisms involved. Immatures were much less dimorphic than adults, but geometric morphometric techniques revealed that head shape sexual differences are already present at this stage. Males and females differed in allometry of all head characters with body size, with males showing a disproportionate increase of head size and dimensions. On the other hand, head dimensions and head shape changed with increasing head size following similar trends in both sexes, possibly indicating developmental restrictions. Consequently, adult sexual dimorphism for head characters in these species is the result of both shape differences in the immature stage and hypermetric growth of the head in relation to body size in males.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 111–124.     

Ecogeographical variation in skull morphometry of howler monkeys (Primates: Atelidae)

Our aim is to identify ecomorphological adaptations in the skull shape of the South American howler monkeys (species of the genus Alouatta, Lacépède, 1799, Primates, Atelidae). Since Alouatta is relatively homogenous in feeding ecology, we expect skull shape variation to be relatively conservative across species. We used geometric morphometrics to quantify craniodental morphology in six species of Alouatta. Multivariate regression, two-block Partial Least Squares, and variation partitioning were used to test for the impact of taxonomy, sexual dimorphism, allometry, geography and climate on skull shape. We found morphological overlap among species and sexes, although some discrimination occurs between species living in seasonal environments as opposed to rain forest species. There was a negative latitudinal gradient in skull size across species, with size explaining 34% of total shape variance. Latitude and climate, though important, were secondary in explaining shape variance. Amazonian Alouatta are larger, have thinner molars, wide incisors, and proportionally larger neurocranium. Overall, the shape of southern species seem well adapted to cope with proportionally tougher food items, whereas Amazonian species seem better equipped to deal with a diet richer in fruits, as confirmed by independent field observations. The small size of Alouatta in the South is possibly linked to the effect of competition with the larger folivorous atelid Brachyteles.     

Size variation facilitates population divergence but does not explain it all: an example study from a widespread African monkey

Subspecific variation is widespread in vertebrates. Within Africa, several mammals have extensive geographic distributions with attendant morphological, ecological, and behavioural variations, which are often used to demarcate subspecies. In the present study, we use a primate species, the vervet monkey, Cercopithecus aethiops, as a case study for intraspecific divergence in widespread mammals, assessed through hard tissue morphology. We examine intraspecific differences in size, shape, and non‐allometric shape from a taxonomic perspective, and discuss the macroevolutionary implications of findings from microevolutionary analyses of geographic variation. A geometric morphometric approach was used, employing 86 three‐dimensional landmarks of almost 300 provenanced crania. Many of the taxonomic differences in skull morphology between vervet populations appear to be related to geographic proximity, with subspecies at opposite extremes of a west‐to‐east axis showing greatest divergence, and populations from central and south Africa being somewhat intermediate. The classification rate from discriminant analyses was lower than that observed in other African primate radiations, including guenons as a whole and red colobus. Nonetheless, taxonomic differences in shape were significant and not simply related to either geography or size. Thus, although shifts in size may be an important first step in adaptation and diversification, with size responding more quickly than shape to environmental change, the six vervet taxa currently recognized (either as species or subspecies) are not simply allometrically scaled versions of one another and are probably best viewed as subspecies. Holding allometry constant when examining inter‐population differences in shape may thus help to reveal the early stages of evolutionary divergence. The vervet case study presented here hence has relevance for future studies examining intraspecific differentiation in other large mammals, particularly through the methods used to identify small but biologically meaningful divergence, with attendant implications for conservation planning. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 823–843.     

Sexual dimorphism of Dall's porpoise and harbor porpoise skulls

To evaluate and quantify sexual dimorphism of skull shape and assess the ontogenetic background for differences, samples of 134 harbor porpoise (Phocoena phocoena) and 85 Dall's porpoise (Phocoenoides dalli) were compared in terms of cranial shape and shape ontogeny using three-dimensional geometric morphometrics. After correction for allometry, no sexual differences were detected in harbor porpoise, while Dall's porpoise showed statistically significant sexual dimorphism of skull shape. Since no sex-specific differences were detected in the directionalities of the ontogenetic vectors, we cannot reject that the dimorphism is innate. Based on the different mating systems of the two species and the lack of sexual dimorphism in the harbor porpoise, the dimorphism in Dall's porpoise is most likely a result of sexual selection in relation physical competition for mates given that male skulls provide room for larger neck muscles with a more favorable lever arm.