Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional Procrustes analysis

Ontogenetic studies of African ape skulls lead to an analysis of morphological differences in terms of allometry, heterochrony, and sexual dimorphism. The use of geometric morphometrics allows us 1) to define size and shape variations as independent factors (an essential but seldom respected condition for heterochrony), and 2) to calculate in percentage of shape changes and to graphically represent the parts of shape variation which are related to various biological phenomena: common allometry, intraspecific allometry, and allometric and nonallometric shape discrimination. Three tridimensional Procrustes analyses and the calculation of multivariate allometries, discriminant functions, and statistical tests are used to compare the skulls of 50 Pan troglodytes, and 50 Gorilla gorilla of different dental stages. The results both complement and modify classical results obtained from similar material but with different methods. Size and Scaling in Primate Morphology, New York: Plenum, p. 175-205). As previously described by Shea, the common growth allometric pattern is very important (64% of total shape variation). It corresponds to a larger increase of facial volume than of neurocranial volume, a more obliquely oriented foramen magnum, and a noticeable reshaping of the nuchal region (higher inion). However, the heterochronic interpretation based on common allometry is rather different from Shea. Gorillas differ from chimpanzees not only with a larger magnitude of allometric change (rate peramorphosis), as is classically said, but also grow more in size than in shape (size acceleration). In other words, for a similar stage of growth, gorillas have the size and shape corresponding to older chimpanzees, and for a similar shape, gorillas have a larger size than chimpanzees. In contrast, sexual dimorphism actually corresponds to allometric changes only, as classically demonstrated (time hypermorphosis). Sexual dimorphism is here significant in adult gorillas alone, and solely in terms of allometry (size-related shape and size, given that sagittal and nuchal crests are not taken into account). The study also permits us to differentiate two different shape variations that are classically confused in ontogenetic studies: a very small part of allometric shape change which is specific to each species (1% of the total shape variation), and nonallometric species-specific traits independent of growth (8% of total shape change). When calculated in terms of intraspecific allometries (including common allometry and noncommon allometry), shape changes are more extensive in gorillas (36% of total shape change) than in chimpanzees (29% of total shape change). The allometric differences mainly concern the inion, which becomes higher; the position of the foramen magnum, more dorsally oriented; and the palate, more tilted in adult gorillas than in adult chimpanzees. In contrast, nonallometric species-specific traits in gorillas are the long and flat vault characterized by a prominent occipital region, the higher and displaced backward glabella, and the protrusive nose. Biomechanical schemes built from shape partition suggest that the increased out-of-plumb position of the head during growth is partially compensated in gorillas by a powerful nuchal musculature due to the peculiar shape of the occipital region.     

Variations and asymmetries in regional brain surface in the genus Homo

Paleoneurology is an important field of research within human evolution studies. Variations in size and shape of an endocast help to differentiate among fossil hominin species whereas endocranial asymmetries are related to behavior and cognitive function. Here we analyse variations of the surface of the frontal, parieto-temporal and occipital lobes among different species of Homo, including 39 fossil hominins, ten fossil anatomically modern Homo sapiens and 100 endocasts of extant modern humans. We also test for the possible asymmetries of these features in a large sample of modern humans and observe individual particularities in the fossil specimens.This study contributes important new information about the brain evolution in the genus Homo. Our results show that the general pattern of surface asymmetry for the different regional brain surfaces in fossil species of Homo does not seem to be different from the pattern described in a large sample of anatomically modern H. sapiens, i.e., the right hemisphere has a larger surface than the left, as do the right frontal, the right parieto-temporal and the left occipital lobes compared with the contra-lateral side. It also appears that Asian Homo erectus specimens are discriminated from all other samples of Homo, including African and Georgian specimens that are also sometimes included in that taxon. The Asian fossils show a significantly smaller relative size of the parietal and temporal lobes. Neandertals and anatomically modern H. sapiens, who share the largest endocranial volume of all hominins, show differences when considering the relative contribution of the frontal, parieto-temporal and occipital lobes. These results illustrate an original variation in the pattern of brain organization in hominins independent of variations in total size. The globularization of the brain and the enlargement of the parietal lobes could be considered derived features observed uniquely in anatomically modern H. sapiens.     

南京2号人类头骨化石的复位和形态

南京2号人类头骨化石仅保留部分的额骨、顶骨、枕骨和颞骨,为一不完整的颅盖骨。其顶骨和枕骨有数条断裂缝,各断块之间有程度不一的错动,致使该颅盖骨显得外形异常。本项研究是对该颅盖骨的错动部分进行复位,结果表明,南京2号头骨有较大的顶骨、较小的上枕鳞相对宽度、可能较大的颅容量。这些形态提示该头骨与直立人有所不同而与早期智人相近。该头骨所具有的角圆枕、颞鳞顶缘形状、枕骨圆枕发育程度、枕骨的枕平面与项平面过渡情况、枕内隆突点与枕外隆突点的距离、头骨骨壁厚度、脑膜中动脉分支情况、头骨枕面观之轮廓线样式等形态细节,还很难作为可靠的依据把南京2号头骨鉴定为直立人。南京2号头骨很大可能是属于智人亚种(Homo sapiens sapiens)中的一员。     

Sexual Selection,Ontogenetic Acceleration,and Hypermorphosis Generates Male Trimorphism in Wellington Tree Weta

Strong sex-specific selection on traits common to both sexes typically results in sexual dimorphism. Here we find that Wellington tree weta (Hemideina crassidens) are sexually dimorphic in both head shape and size due to differential selection pressures on the sexes: males use their heads in male-male combat and feeding whereas females use theirs for feeding only. Remarkably, the sexes share a common ontogenetic trajectory with respect to head growth. Male head shape allometry is an extension of the female’s trajectory despite maturing two instars earlier, a feat achieved through ontogenetic acceleration and hypermorphosis. Strong sexual selection also favours the evolution of alternative reproductive strategies in which some males produce morphologically different weapons. Wild-caught male H. crassidens are trimorphic with regard to weapon size, a rare phenomenon in nature, and weapon shape is related to each morph’s putative mating strategy.     

A new species of sculpin,Icelus ecornis (Scorpaeniformes: Cottidae) from the southwestern Okhotsk Sea

A new cottid species,Icelus ecornis, is described on the basis of 31 specimens collected from 159–226 m in the southwestern Okhotsk Sea off Hokkaido, Japan. It is distinguished from all other members of the genusIcelus by the following combination of characters: no supraocular and parietal spines; short blunt nuchal spine; cirri absent from head and body, except for supraocular, parietal and nuchal regions; platelike scales of dorsal row bearing 6–10 long uniform spinules; tubular lateral line scales bearing small spines on dorsal and posterior margins; large oval black spot on first dorsal fin; 16–20 anal fin rays.     

Sexual selection on forelimb muscles of western grey kangaroos (Skippy was clearly a female)

Studies of sexual selection have tended to concentrate on obvious morphological dimorphisms such as crests, horns, antlers, and other physical displays or weapons; however, traits that show no obvious sexual dimorphism may nevertheless still be under sexual selection. Sexual selection theory generally predicts positive allometry for sexually selected traits. When fighting, male kangaroos use their forelimbs to clasp and hold their opponent and, standing on their tail, bring up their hind legs to kick their opponent. This action requires substantial strength and balance. We examined allometry of forelimb musculature in male and female western grey kangaroos (Macropus fuliginosus) to determine whether selection through male–male competition is associated with sex differences in muscle development. Forelimbs of males are more exaggerated than in females, with relatively greater muscle mass in males than the equivalent muscles in females. Furthermore, while muscles generally showed isometric growth in female forelimbs, every muscle demonstrated positive allometry in males. The significant positive allometry in male forelimb musculature, particularly those muscles most likely involved in male–male combat (a group of muscles involved in grasping: shoulder adduction, elbow flexion; and pulling: arm retraction, elbow flexion), clearly suggests that this musculature is subject to sexual selection. In addition to contributing to locomotion, the forelimbs of male kangaroos can also act as a signal, a weapon, and help in clasping, features that would contribute towards their importance as a sexually selected trait. Males would therefore benefit from well‐developed musculature of the arms and upper body during competition for mates. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 923–931.     

A reassessment of the cranial morphology of Neoepiblema acreensis (Rodentia: Chinchilloidea), a Miocene rodent from South America

The rodent Neoepiblema acreensis (Chinchilloidea: Neoepiblemidae) is member of a lineage that reached gigantic dimensions during the Late Miocene of South America—the Neoepiblemidae. In this paper, the cranial anatomy of this rodent is reviewed. Noninvasive imaging is used to reveal internal structures. Our review is based mainly on an almost complete cranium from the Upper Miocene deposits of the western Amazonia of Brazil. The cranium has an elongated rostrum, large frontal sinuses, a deep temporal fossa, well-developed sagittal, nuchal, medial occipital, and secondary crests, and a tympanic fenestra connected to the external acoustic meatus by a thin ventral cleft. Remarkably, the cranium shows the presence of fossae on the posterior region of the frontal and parietal bones, and a “W-shaped” fronto-parietal suture, which are not present in other analyzed chinchilloids. This study contributes to the knowledge of the morphology of this extinct rodent as well as to the phylogenetic relationships and paleobiology of neoepiblemids.     

Does compensatory growth modify fish scale shape?

Although the shape of fish scales is useful for determining stock membership, the role of extrinsic (e.g. habitat, food type) and intrinsic (e.g. growth) factors in determining variation in fish scales shape has not been determined. This study examined whether fish scale shape changes as a result of compensatory growth in juveniles of the cyprinid roach, Rutilus rutilus (L.) reared on a fish farm in the UK. This was analyzed using geometric morphometric methods. Sufficient evidence was generated to accept the assumption that food availability and type between different growing-out facilities resulted in compensatory growth and this was sufficient to cause scale shape differences. This was tested using multivariate analysis of variance (MANOVA) analysis with the principal components scores of specimens (PCs) as dependent variables, to investigate whether fish scale shape (where the configuration of landmark coordinates were scaled, translated and rotated) form (where the configuration of landmark coordinates were translated and rotated not scaled) and allometry free (allometrically adjusting scale shape according to length) are related to holding facility (as fixed factor). Cross validated discriminant analysis was used to assess and compare the efficacy of shape, form and allometry free information. Identification rates are much better than chance with allometry free and shape alone, and classification is improved when size is taken into account.     

A new cottid species, Icelus sekii (Perciformes: Cottoidei), from Hokkaido, Japan

A new cottid species, Icelus sekii, is described on the basis of six specimens collected from off Rausu and Urakawa, Hokkaido Island, Japan. This species is distinguished from its congeners by the following combination of characters: supraocular and parietal spines absent; nuchal spine obscure; uppermost preopercular spine unbranched; no scales between dorsal scale row and lateral line scale row, and no scales below lateral line scale row; supraocular, parietal, and nuchal cirri present; five dark brown saddles dorsolaterally; anal fin rays 13; pectoral fin rays 15; vertebrae 12 + 24–25 = 36–37. Icelus sekii can be mature at the smallest size among the species of Icelus. As a secondary sexual character, the male holotype has unique ensiform flaps on the distal tips of the first dorsal fin.     

SEX‐SPECIFIC PATTERNS OF MORPHOLOGICAL DIVERSIFICATION: EVOLUTION OF REACTION NORMS AND STATIC ALLOMETRIES IN NERIID FLIES

The consequences of sex‐specific selection for patterns of diversification remain poorly known. Because male secondary sexual traits are typically costly to express, and both costs and benefits are likely to depend on ambient environment and individual condition, such traits may be expected to diversify via changes in reaction norms as well as the scaling of trait size with body size (static allometry). We investigated morphological diversification within two species of Australian neriid flies (Telostylinus angusticollis, Telostylinus lineolatus) by rearing larvae from several populations on larval diets varying sixfold in nutrient concentration. Mean body size varied among populations of T. angusticollis, but body size reaction norms did not vary within either species. However, we detected diversification of reaction norms for body shape in males and females within both species. Moreover, unlike females, males also diversified in static allometry slope and reaction norms for static allometry slope of sexual and nonsexual traits. Our findings reveal qualitative sex differences in patterns of morphological diversification, whereby shape–size relationships diversify extensively in males, but remain conserved in females despite extensive evolution of trait means. Our results highlight the importance of incorporating plasticity and allometry in studies of adaptation and diversification.     

Functional morphology of the asterionic region in extant hominoids and fossil hominids

Asterionic sutural patterns in Plio-Pleistocene hominid crania have never been examined in detail. We present an analysis of this anatomical region in Australopithecus and Homo and relate different sutural patterns to functional changes in the masticatory apparatus. The great apes and A. afarensis share the common adult higher primate sutural pattern referred to as the "asterionic notch," which develops in response to the hypertrophy of posterior temporalis muscle fibers and the consequent formation of compound temporal/nuchal crests. This sutural configuration also appears to be present on the early Homo cranium KNM-ER 1805. In contrast, adult male A. boisei crania exhibit a unique pattern where the temporal squama overlaps the parietal which, in turn, overlaps the par mastoidea and the upper scale of the occipital bone. We relate this arrangement to the need to reinforce the rear of a thin-walled braincase against the net tensile forces exerted by the temporalis and nuchal muscles. The common juvenile hominoid edge-to-edge asterionic articulation is maintained in adult A. africanus, A. robustus, female A. boisei, and most Homo crania. We discuss the latter pattern in regard to anterior temporalis hypertrophy in A. africanus, A. robustus, and A. boisei and to craniofacial paedomorphosis in Homo.     

Allometry, bilateral asymmetry and sexual differences in the vocal tract of common eiders Somateria mollissima and king eiders S. spectabilis

Intraspecific sexual differences, high variation, and positive allometry of sexually-selected external display structures are common. Many sexually-selected anatomical specializations occur in the avian vocal tract but intraspecific variation and allometry have been investigated little. The tracheal bulla bulla syringealis occurs in males of most duck species. We quantified variation and size-scaling of the bulla, plus sexual differences in size of trachea, bronchi, and vocal muscles, for 62 common eiders Somateria mollissima and 51 king eiders S. spectabilis. Trends were similar in both species. Bullar ossification and definitive size occurred early in life: bullar size did not differ between first-year and older males. Bullar size did not vary more than size of other body parts (CVs of 3.4–7.0% for bullar length and breadth). Bullar size scaled to body size with negative allometry or isometry. Vocal muscles were 10–50% thicker in males than females, a much greater sexual difference than in body size (CVs of 3–6% on linear body-size variables). Vocal muscles were larger on the left side in both sexes and bilateral asymmetry was slightly more pronounced in males. Low variation and a trend towards negative allometry suggest that bullar size is under stabilizing selection; if bullar size affects vocal attributes of voice, then the latter cannot be condition-dependent. We recommend comparative research on vocal communication, vocal individuality and vocal-tract anatomy and function in eiders and other ducks.     

The sixth skull cap of Pithecanthropus erectus

The sixth skull cap of Pithecanthropus erectus (or skull V, since the Modjokerto skull has not been given a number) was found in the upper layers of the Trinil beds of Sangiran (Central Java) in 1963, associated with fossils of the Sino-Malayan fauna. No stone tools were discovered in direct association with the find. The specimen consists of the occipital, both parietals, both temporals, sphenoid fragments, the frontal and the left zygomatic bone. We consider the skull to be a male in his early twenties. The occipital, parietal, frontal and temporal bones demonstrate definite pithecanthropine characteristics, and the cranial capacity is estimated to be 975 cm³. Of the superstructures, the supraorbital torus is extraodinarily thick, approaching the condition in Australopithecus boisei and Rhodesian man. And the sagittal torus is certainly higher than in skulls I and II, but lower than in skull IV. In addition, the angle between the occipital and nuchal planes is larger than in the previous finds. As revealed by various features, the gap between the robustness of skull IV on one hand, and skulls I, II and III on the other, is bridged by the present find. There is no reasonable taxonomic need to ascribe this specimen to a new species, because it seems to be merely an intrapopulational variant of the same species. Other skulls of P. erectus suggest that the bregmatic eminence, and hence the vertex, is invariably situated at bregma, but this new skull cap deviates from the pattern. Its pteric regions disclose the anthropoid X and I types. The middle meningeal groove pattern is similar to other Pithecanthropus skulls; however, it betrays a known anomaly in that the main stem is covered for a short distance by a bony plate. The mastoid process is fairly well developed, and is also well pneumatized as in P. pekinensis, with its air cells invading the pronounced supramastoid crest. The zygomatic bone, the first one recovered of P. erectus, does not show characters of particular importance. In fact, its thickness is in the range of modern man. We would like to stress that the absence of the cranial base does not necessarily indicate that the specimen must be a poor victim of cannibalism, since the morphology of the base renders it more susceptible to post-mortem natural traumata.     

Thin-plate spline analysis of allometry and sexual dimorphism in the human craniofacial complex

The relationship between allometry and sexual dimorphism in the human craniofacial complex was analyzed using geometric morphometric methods. Thin-plate splines (TPS) analysis has been applied to investigate the lateral profile of complete adult skulls of known sex. Twenty-nine three-dimensional (3D) craniofacial and mandibular landmark coordinates were recorded from a sample of 52 adult females and 52 adult males of known age and sex. No difference in the influence of size on shape was detected between sexes. Both size and sex had significant influences on shape. As expected, the influence of centroid size on shape (allometry) revealed a shift in the proportions of the neurocranium and the viscerocranium, with a marked allometric variation of the lower face. Adjusted for centroid size, males presented a relatively larger size of the nasopharyngeal space than females. A mean-male TPS transformation revealed a larger piriform aperture, achieved by an increase of the angulation of the nasal bones and a downward rotation of the anterior nasal floor. Male pharynx expansion was also reflected by larger choanae and a more posteriorly inclined basilar part of the occipital clivus. Male muscle attachment sites appeared more pronounced. In contrast, the mean-female TPS transformation was characterized by a relatively small nasal aperture. The occipital clivus inclined anteriorly, and muscle insertion areas became smoothed. Besides these variations, both maxillary and mandibular alveolar regions became prognathic. The sex-specific TPS deformation patterns are hypothesized to be associated with sexual differences in body composition and energetic requirements.     

枕骨三维形态在现生人群间的变异

与面颅、脑颅和颅底不同,枕骨与人群间遗传信息的关系不明确且研究较少。传统形态测量方法对枕骨的研究难以全面反映枕骨的形态信息。为更加精细地探究枕骨形态与人群的关系,本文以亚洲、非洲和欧洲地区的103例现生男性头骨为研究对象,通过三维几何形态测量和多元统计分析的方法对枕骨三维形态和异速生长模式在人群间的差异进行了研究。研究结果表明,枕骨的大小和形状在现生人群中具有显著差异,然而这种差异并不足以区分不同人群。现代人枕骨的三维形态具有较大的变异,主要表现在枕外隆凸点的突出程度、上下相对位置以及枕平面与项平面的比例,其次表现在星点位置在前后、内外以及上下方向上的变化,斜坡的倾角变化等方面。异速生长的分析表明,不同人群中存在不同的异速生长模式,但是非洲和欧洲人群也存在相似的趋势。本研究认为枕骨三维形态在反映人群间遗传关系上作用较小,支持枕骨形态可能更多受到功能和环境等因素的影响。     

Body shape variation in the Characid Psalidodon rivularis from São Francisco river,Southeast Brazil (Characiformes: Stethaprioninae)

Psalidodon rivularis is a species of tetra endemic to the São Francisco River basin and, based on cytogenetic and molecular studies, represents a complex of species. The objective of the present work was to identify morphological differences in the body shape of seven populations of P. rivularis from the Upper and Middle São Francisco River basin through geometric morphometry. In all, we photographed 174 individuals on the right side of the body and 17 landmarks were digitized on each image. To study the effects of allometry on the shape, we performed regression analysis and, to study shape modulation at different collection points and sub-basins, the canonical variation analyses. We found differences in shape between collection points and sub-basins associated with relative body height and sub-orbital plate recoil, in addition to a significant influence of size on specimen shape (allometry) associated with the ventral skull, orbits and sub-orbital plate. We do not envision differences in body shape between males and females. Several works with fish relate body height with water velocity, while the sub-orbital plate recoil shows a taxonomic or ecological potential, marking the main difference between the populations of the Upper and Middle São Francisco River.     

Sexual differences in head form and diet in a population of Mexican lance‐headed rattlesnakes,Crotalus polystictus

Sexual dimorphism of phenotypic traits associated with resource use is common in animals, and may result from niche divergence between sexes. Snakes have become widely used in studies of the ecological basis of sexual dimorphism because they are gape‐limited predators and their head morphology is likely to be a direct indicator of the size and shape of prey consumed. We examined sexual dimorphism of body size and head morphology, as well as sexual differences in diet, in a population of Mexican lance‐headed rattlesnakes, Crotalus polystictus, from the State of México, Mexico. The maximum snout–vent length of males was greater than that of females by 21%. Males had relatively larger heads, and differed from females in head shape after removing the effects of head size. In addition, male rattlesnakes showed positive allometry in head shape: head width was amplified, whereas snout length was truncated with increased head size. By contrast, our data did not provide clear evidence of allometry in head shape of females. Adults of both males and females ate predominately mice and voles; however, males also consumed a greater proportion of larger mammalian species, and fewer small prey species. The differences in diet correspond with dimorphism in head morphology, and provide evidence of intersexual niche divergence in the study population. However, because the sexes overlapped greatly in diet, we hypothesize that diet and head dimorphisms in C. polystictus are likely related to different selection pressures in each sex arising from pre‐existing body size differences rather than from character displacement for reducing intersexual competition. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 633–640.     

Modifications in call characteristics and sonic apparatus morphology during puberty in Ophidion rochei (actinopterygii: Ophidiidae)

Juveniles, females, and males of Ophidion rochei share similar external morphology, probably because they are mainly active in the dark, which reduces the role of visual cues. Their internal sonic apparatuses, however, are complex: three pairs of sonic muscles, and highly modified vertebrae and ribs are involved in sound production. The sonic apparatus of males differs from juveniles and females in having larger swimbladder plates (modified ribs associate with the swimbladder wall) and sonic muscles, a modified swimbladder shape and a mineralized structure called the “rocker bone” in front of the swimbladder. All of these male traits appear at the onset of sexual maturation. This article investigates the relationship between morphology and sounds in male O. rochei of different sizes. Despite their small size range total length (133–170 mm TL), the five specimens showed pronounced differences in sound‐production apparatus morphology, especially in terms of swimbladder shape and rocker bone development. This observation was reinforced by the positive allometry measured for the rocker bone and the internal tube of the swimbladder. The differences in morphology were related to marked differences in sound characteristics (especially frequency and pulse duration). These results suggest that male calls carry information about the degree of maturity. Deprived of most visual cues, ophidiids probably have invested in other mechanisms to recognize and distinguish among individual conspecifics and between ophidiid species. As a result, their phenotypes are externally similar but internally very different. In these taxa, the great variability of the sound production apparatus means this complex system is a main target of environmental constraints. J. Morphol. 275:650–660, 2014. © 2014 Wiley Periodicals, Inc.     

Social Dispersion and Genetic Variation in Two Species of Emballonurid Bats

Saccopteryx leptura and S. bilineata are closely related, sympacric species of neotropical bats that exhibit marked differences in social organization and dispersion patterns. S. leptura is monogamous and roosts in small groups of 1 to 5 (Y = 2.6) individuals that are finely dispersed. S. bilineata is harem-polygamous and roosts in larger groups of 1 to 42 (Y = 8.1) individuals that are more coarsely dispersed. Allozyme genetic studies of individuals from Trinidad, W I. demonstrate that both species carry similar, high levels of polymorphism and heterozygosity. Although significant genetic heterogeneity was observed among geographical populations of S. leptura, there is no evidence for either species that social structuring leads to inbreeding and the loss of heterozygosity, or that it promotes the development of genetic heterogeneity among social units that could accelerate the evolutionary diversification of these taxa. These results do not support a recently proposed hypothesis that social structuring in mammals has these effects. Observed intercolony genetic heterogeneity among adult males resident in multimale groups of S. bilineata is greater than intercolony heterogeneity of adult females. This is an apparent result of female dispersal and the recruitment of males into their parental groups. These results suggest that the adult males within large colonies may be kin-related.