Evolution of the Mammalian Neck from Developmental,Morpho-Functional,and Paleontological Perspectives

The mammalian neck adopts a variety of postures during daily life and generates numerous head trajectories. Despite its functional diversity, the neck is constrained to seven cervical vertebrae in (almost) all mammals. Given this low number, an unexpectedly high degree of modularity of the mammalian neck has more recently been uncovered. This work aims to review neck modularity in mammals from a developmental, morpho-functional, and paleontological perspective and how high functional diversity evolved in the mammalian neck after the occurrence of meristic limitations. The fixed number of cervical vertebrae and the developmental modularity of the mammalian neck are closely linked to anterior Hox genes expression and strong developmental integration between the neck and other body regions. In addition, basic neck biomechanics promote morpho-functional modularity due to preferred motion axes in the cranio-cervical and cervico-thoracic junction. These developmental and biomechanical determinants result in the characteristic and highly conserved shape variation among the vertebrae that delimits morphological modules. The step-wise acquisition of these unique cervical traits can be traced in the fossil record. The increasing functional specialization of neck modules, however, did not evolve all at once but started much earlier in the upper than in the lower neck. Overall, the strongly conserved modularity in the mammalian neck represents an evolutionary trade-off between the meristic constraints and functional diversity. Although a morpho-functional partition of the neck is common among amniotes, the degree of modularity and the way neck disparity is realized is unique in mammals.

     

Head‐turning morphologies: Evolution of shape diversity in the mammalian atlas–axis complex

Mammals flex, extend, and rotate their spines as they perform behaviors critical for survival, such as foraging, consuming prey, locomoting, and interacting with conspecifics or predators. The atlas–axis complex is a mammalian innovation that allows precise head movements during these behaviors. Although morphological variation in other vertebral regions has been linked to ecological differences in mammals, less is known about morphological specialization in the cervical vertebrae, which are developmentally constrained in number but highly variable in size and shape. Here, we present the first phylogenetic comparative study of the atlas–axis complex across mammals. We used spherical harmonics to quantify 3D shape variation of the atlas and axis across a diverse sample of species, and performed phylogenetic analyses to investigate if vertebral shape is associated with body size, locomotion, and diet. We found that differences in atlas and axis shape are partly explained by phylogeny, and that mammalian subclades differ in morphological disparity. Atlas and axis shape diversity is associated with differences in body size and locomotion; large terrestrial mammals have craniocaudally elongated vertebrae, whereas smaller mammals and aquatic mammals have more compressed vertebrae. These results provide a foundation for investigating functional hypotheses underlying the evolution of neck morphologies across mammals.     

Adaptive divergence of scaling relationships mediates the arms race between a weevil and its host plant

Coevolution of exaggerated morphologies between insects and plants is a well-known but poorly understood phenomenon in evolutionary biology. In the antagonistic interaction between a seed-predatory insect, the camellia weevil (Curculio camelliae), and its host plant, Japanese camellia (Camellia japonica), we examined the evolutionary trajectory of an exaggerated offensive trait of the weevil (rostrum length) in terms of scaling relationship. Sampling throughout Japan revealed that the ratio of the rostrum length to overall body size was correlated with the ratio of the pericarp thickness to overall fruit size across the localities. We found a geographical interpopulation divergence in a parameter pertaining to the allometric equation of rostrum length (the coefficient a in y=axb, where y and x denote rostrum and body lengths, respectively), and the pattern of geographical differentiation in the allometric coefficient was closely correlated with the variation in the pericarp thickness of Japanese camellia. Our results provide a novel example of a geographically diverged scaling relationship in an insect morphology resulting from a coevolutionary arms race with its host plant.     

Axial allometry in a neutrally buoyant environment: effects of the terrestrial‐aquatic transition on vertebral scaling

Ecological diversification into new environments presents new mechanical challenges for locomotion. An extreme example of this is the transition from a terrestrial to an aquatic lifestyle. Here, we examine the implications of life in a neutrally buoyant environment on adaptations of the axial skeleton to evolutionary increases in body size. On land, mammals must use their thoracolumbar vertebral column for body support against gravity and thus exhibit increasing stabilization of the trunk as body size increases. Conversely, in water, the role of the axial skeleton in body support is reduced, and, in aquatic mammals, the vertebral column functions primarily in locomotion. Therefore, we hypothesize that the allometric stabilization associated with increasing body size in terrestrial mammals will be minimized in secondarily aquatic mammals. We test this by comparing the scaling exponent (slope) of vertebral measures from 57 terrestrial species (23 felids, 34 bovids) to 23 semi‐aquatic species (pinnipeds), using phylogenetically corrected regressions. Terrestrial taxa meet predictions of allometric stabilization, with posterior vertebral column (lumbar region) shortening, increased vertebral height compared to width, and shorter, more disc‐shaped centra. In contrast, pinniped vertebral proportions (e.g. length, width, height) scale with isometry, and in some cases, centra even become more spool‐shaped with increasing size, suggesting increased flexibility. Our results demonstrate that evolution of a secondarily aquatic lifestyle has modified the mechanical constraints associated with evolutionary increases in body size, relative to terrestrial taxa.     

Dichotomy of eutherian reproduction and metabolism

How anatomical, physiological and ecological (life history) features scale with body mass is a fundamental question in biology. There is an ongoing debate in the scientific literature whether allometric scaling follows a universal pattern that can be described in a single model, or differs between groups. However, recently some analyses were published demonstrating a change in scaling across the body mass range: brain‐size allometry of mammals indicates that scaling follows a curvilinear pattern in double‐logarithmic space, and a quadratic pattern in double‐logarithmic space was found in one of the largest physiological datasets, on basal metabolic rate (MR) in mammals. Here, we analysed a variety of independent datasets on anatomical, physiological and ecological characteristics in mammals, birds and reptiles to answer the question whether the quadratic scaling is a universal biological law, or a pattern unique to mammals. The pattern was present in mammalian basal and field MR, brain size, and reproduction parameters, but neither in other organ allometries in mammals, nor in the scaling of MR in birds and reptiles. However, the curvature was better explained by separate allometric scaling of three different mammalian reproduction strategies: marsupials, and eutherian mammals with one and with many offspring. The two latter strategies are distributed unequally over the body mass range in eutherian mammals. Our findings show that a quadratic model, as well as a traditional allometric model with a universal scaling exponent (such as 0.67 or 0.75), may be inappropriate in mammals as they are a result of different scalings within these three reproductive groups. We propose that the observed distribution pattern is the result of the eutherian mammal clade's uniquely pronounced dichotomy of reproductive strategies.     

The evolution of ontogenetic allometric trajectories in mammalian domestication

Morphological divergence of domesticated as compared to wild forms must result from changes in the ontogenetic process. Species‐specific tests for heterochrony have rejected a single explanation of domestic forms representing juveniles of their wild relatives. Ontogenetic allometric trajectories for 12 pairs of wild and domestic mammals were examined using skull growth data for 1070 specimens, including representatives from all lineages in which domestication has occurred. A suite of tests were performed to quantify allometric disparity in wild and domestic forms and assess the extent and patterning of modification to allometric trajectories. Domestication has modified postnatal ontogenetic allometric trajectories in mammals, and has generated disparity, achieved through lengthening of trajectory slopes and alteration to slope angles. Allometric disparity was similar for domestic forms compared to their wild relatives, whereas the magnitude of dispersion along allometric vectors differed between precocial mammals and altricial mammals, underscoring the importance of life history and shared evolutionary history in patterns of ontogenetic variation. The results verify the importance of scaling in the morphological changes associated with domestication. The response to domestication for all measured trajectory parameters was variable across species, suggesting multiple pathways of change.     

Patterns of growth in the presacral vertebral column of the leopard gecko (Eublepharis macularius)

Postnatal growth patterns within the vertebral column may be informative about body proportions and regionalization. We measured femur length, lengths of all pre‐sacral vertebrae, and lengths of intervertebral spaces, from radiographs of a series of 21 Eublepharis macularius, raised under standard conditions and covering most of the ontogenetic body size range. Vertebrae were grouped into cervical, sternal, and dorsal compartments, and lengths of adjacent pairs of vertebrae were summed before analysis. Femur length was included as an index of body size. Principal component analysis of the variance‐covariance matrix of these data was used to investigate scaling among them. PC1 explained 94.19% of total variance, interpreted as the variance due to body size. PC1 differed significantly from the hypothetical isometric vector, indicating overall allometry. The atlas and axis vertebrae displayed strong negative allometry; the remainder of the vertebral pairs exhibited weak negative allometry, isometry or positive allometry. PC1 explained a markedly smaller amount of variance for the vertebral pairs of the cervical compartment than for the remainder of the vertebral pairs, with the exception of the final pair. The relative standard deviations of the eigenvalues from the PCAs of the three vertebral compartments indicated that the vertebrae of the cervical compartment were less strongly integrated by scaling than were the sternal or dorsal vertebrae, which did not differ greatly between themselves in their strong integration, suggesting that the growth of the cervical vertebrae is constrained by the mechanical requirements of the head. Regionalization of the remainder of the vertebral column is less clearly defined but may be associated with wave form propagation incident upon locomotion, and by locomotory changes occasioned by tail autotomy and regeneration. Femur length exhibits negative allometry relative to individual vertebral pairs and to vertebral column length, suggesting a change in locomotor requirements over the ontogenetic size range.     

Energetic benefits and adaptations in mammalian limbs: Scale effects and selective pressures

Differences in limb size and shape are fundamental to mammalian morphological diversity; however, their relevance to locomotor costs has long been subject to debate. In particular, it remains unknown if scale effects in whole limb morphology could partially underlie decreasing mass‐specific locomotor costs with increasing limb length. Whole fore‐ and hindlimb inertial properties reflecting limb size and shape—moment of inertia (MOI), mass, mass distribution, and natural frequency—were regressed against limb length for 44 species of quadrupedal mammals. Limb mass, MOI, and center of mass position are negatively allometric, having a strong potential for lowering mass‐specific locomotor costs in large terrestrial mammals. Negative allometry of limb MOI results in a 40% reduction in MOI relative to isometry's prediction for our largest sampled taxa. However, fitting regression residuals to adaptive diversification models reveals that codiversification of limb mass, limb length, and body mass likely results from selection for differing locomotor modes of running, climbing, digging, and swimming. The observed allometric scaling does not result from selection for energetically beneficial whole limb morphology with increasing size. Instead, our data suggest that it is a consequence of differing morphological adaptations and body size distributions among quadrupedal mammals, highlighting the role of differing limb functions in mammalian evolution.     

The giraffe (Giraffa camelopardalis) cervical vertebral column: a heuristic example in understanding evolutionary processes?

The current study considers the osteological morphology of the giraffe (Giraffa camelopardalis) vertebral column, with emphasis on evaluating both the adaptive and constraining features compared with other ungulates as a heuristic example in understanding evolutionary processes. Vertebral columns of giraffes varying in age from calf to adult were studied in order to understand the potential evolutionary scenarios that might have led to the modern phenotype. Data from the giraffe sample were then compared with the results from several other ungulate species, including the okapi and two species of camelids that also have visibly elongated necks. Our results show that the elongated neck of the modern giraffe appears to specifically result from evolutionary changes affecting the seven cervical vertebrae, independent of the remainder of the vertebral column. The cervical vertebrae comprise over half of the length of the total vertebral column in the giraffe. The increases in cervical vertebrae lengths also appear to be allometrically constrained, with alterations in the overall length of the neck resulting from the elongation of the entire cervical series, rather than from a single vertebra or subset of vertebrae. We place our results in the context of hypotheses concerning the origin and evolution of the giraffe neck, and the evolution of long necks in a broader sense. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155 , 736–757.     

Effects of allometry,productivity and lifestyle on rates and limits of body size evolution

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow–fast life-history continuum, and the allometric scaling of generation time to predict a clade''s evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow–fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.     

Shared extremes by ectotherms and endotherms: Body elongation in mustelids is associated with small size and reduced limbs

An elongate body with reduced or absent limbs has evolved independently in many ectothermic vertebrate lineages. While much effort has been spent examining the morphological pathways to elongation in these clades, quantitative investigations into the evolution of elongation in endothermic clades are lacking. We quantified body shape in 61 musteloid mammals (red panda, skunks, raccoons, and weasels) using the head‐body elongation ratio. We also examined the morphological changes that may underlie the evolution toward more extreme body plans. We found that a mustelid clade comprised of the subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae exhibited an evolutionary transition toward more elongate bodies. Furthermore, we discovered that elongation of the body is associated with the evolution of other key traits such as a reduction in body size and a reduction in forelimb length but not hindlimb length. This relationship between body elongation and forelimb length has not previously been quantitatively established for mammals but is consistent with trends exhibited by ectothermic vertebrates and suggests a common pattern of trait covariance associated with body shape evolution. This study provides the framework for documenting body shapes across a wider range of mammalian clades to better understand the morphological changes influencing shape disparity across all vertebrates.     

The Allometry of primate skeletal weight

There is a widely held assumption that skeletal weights of mammals increase disproportionately with increased body size. Recent empirical studies have supported this assumption, and it has been suggested that this might account for the fact that metabolic rate scales to body weight with a negative allometry. Other studies, however, have suggested that skeletal weight in primates is directly proportionate to body weight. The results of this study support this latter interpretation and also indicate that the same is true for two other orders of mammals that were a part of the earlier allometric studies. The evidence suggests that skeletal weight scales isometricallywith body weight within individual mammalian orders. From this it is concluded that skeletal weight does not play any part in determining the negatively allometric scaling of metabolic rate.     

Ontogenic growth of the haemopoietic stem cell pool in humans

Recently, the size of the active stem cell pool has been predicted to scale allometrically with the adult mass of mammalian species with a 3/4 power exponent, similar to what has been found to occur for the resting metabolic rate across species. Here we investigate the allometric scaling of human haemopoietic stem cells (HSCs) during ontogenic growth and predict a linear scaling with body mass. We also investigate the allometric scaling of resting metabolic rate during growth in humans and find a linear scaling with mass similar to that of the haemopoietic stem cell pool. Our findings suggest a common underlying organizational principle determining the linear scaling of both the stem cell pool and resting metabolic rate with mass during ontogenic growth within the human species, combined with a 3/4 scaling with adult mass across mammalian species. It is possible that such common principles remain valid for haemopoiesis in other mammalian species.     

Static allometry of mammalian teeth and the correlation of tooth size and body size in contemporary mammals

Functional least squares regression was used to fit the allometric equation, y = bx^k, to data on head-body lengths and body weights for 123 species of mammals. These measurements were found to be highly correlated and to scale isometrically. The scaling of M ₁ area with head-body length was investigated for 288 species of terrestrial mammals. A method was described for estimating the body size of extinct mammals from M ₁ area and the tooth size-body size relationships discovered among contemporary forms.     

Sexual dimorphism and ontogenetic allometry of soft tissues in Rattus norvegicus.

Most studies of sexual dimorphism in mammals focus on overall body size. However, relatively little is known about the differences in growth trajectories that produce dimorphism in organ and muscle size. We weighed six organs and four muscles in Rattus norvegicus to determine what heterochronic and allometric scaling differences exist between the sexes. This cross-sectional growth study included 113 males and 109 females with ages ranging from birth to 200 days of age. All muscle and organ weights were ultimately greater in males than in females, because males grew for a longer period of time, had a greater maximum rate of growth, and spent more time near the maximum rate. No ontogenetic scaling differences existed between the sexes in organ weight except for lungs and gonads. During growth, organ weights were negatively allometric to body weight. No scaling differences relative to body weight existed between the sexes for muscles; however, there was variation in the allometric relations among muscles relative to body weight. Sexual dimorphism in muscles and organs appears to be a size difference resulting from differences in the duration and rates of growth.     

Extreme selection in humans against homeotic transformations of cervical vertebrae

Abstract Why do all mammals, except for sloths and manatees, have exactly seven cervical vertebrae? In other vertebrates and other regions, the vertebral number varies considerably. We investigated whether natural selection constrains the number of cervical vertebrae in humans. To this end, we determined the incidence of cervical ribs and other homeotic vertebral changes in radiographs of deceased human fetuses and infants, and analyzed several existing datasets on the incidence in infants and adults. Our data show that homeotic transformations that change the number of cervical vertebrae are extremely common in humans, but are strongly selected against: almost all individuals die before reproduction. Selection is most probably indirect, caused by a strong coupling of such changes with major congenital abnormalities. Changes in the number of thoracic vertebrae appear to be subject to weaker selection, in good correspondence with the weaker evolutionary constraint on these numbers. Our analysis highlights the role of prenatal selection in the conservation of our common body plan.     

BODY AND LIMB SIZE DISSOCIATION AT THE ORIGIN OF BIRDS: UNCOUPLING ALLOMETRIC CONSTRAINTS ACROSS A MACROEVOLUTIONARY TRANSITION

The origin of birds and powered flight is a classic major evolutionary transition. Research on their origin often focuses on the evolution of the wing with trends of forelimb elongation traced back through many nonavian maniraptoran dinosaurs. We present evidence that the relative forelimb elongation within avian antecedents is primarily due to allometry and is instead driven by a reduction in body size. Once body size is factored out, there is no trend of increasing forelimb length until the origin of birds. We report that early birds and nonavian theropods have significantly different scaling relationships within the forelimb and hindlimb skeleton. Ancestral forelimb and hindlimb allometric scaling to body size is rapidly decoupled at the origin of birds, when wings significantly elongate, by evolving a positive allometric relationship with body size from an ancestrally negative allometric pattern and legs significantly shorten by keeping a similar, near isometric relationship but with a reduced intercept. These results have implications for the evolution of powered flight and early diversification of birds. They suggest that their limb lengths first had to be dissociated from general body size scaling before expanding to the wide range of fore and hindlimb shapes and sizes present in today's birds.     

Modes of ontogenetic allometric shifts in crocodylian vertebrae

During postnatal ontogeny of vertebrates, allometric trends in certain morphological units or dimensions can shift drastically among isometry, positive allometry, and negative allometry. However, detailed patterns of allometric transitions in certain timings have not been explored well. Identifying the presence and nature of allometric shifts is essential for understanding the patterns of changes in relative size and shape and the proximal factors that are controlling these changes mechanistically. Allometric trends in 10 selected vertebrae (cervical 2–caudal 2) from hatchlings to very mature individuals of Alligator mississippiensis (Archosauria, Crocodylia) are reported in the present study. Allometric coefficients in 12 vertebral dimensions are calculated and compared relative to total body length, including centrum, neural spine, transverse process, zygapophysis, and neural pedicle. During the postnatal growth, positive allometry is the most common type of relative change (10 of the 12 dimensions), although the diameter of the neural canal shows a negative allometric trend. However, when using spurious breaks (i.e. allometric trends subdivided into growth stages using certain growth events, and key body sizes and/or ages), vertebral parts exhibit various pathways of allometric shifts. Based on allometric trends in three spurious breaks, separated by the end of endochondral ossification (body length: approximnately 0.9 m), sexual maturity (1.8 m), and the stoppage of body size increase (2.8 m), six types of ontogenetic allometric shifts are established. Allometric shifts exhibit a wide range from positive allometry restricted only in the early postnatal stage (Type I) to life‐long positive allometry (Type VI). This model of ontogenetic allometric shifts is then applied to interpret potential mechanisms (causes) of allometric changes, such as (1) growth itself (when allometric trend gradually decreases to isometric or negative allometric change: Type II–IV allometric shift); (2) developmental constraint (when positive allometry is limited only in the early growth stage: Type I allometric shift); and (3) functional or biomechanical drive (when positive allometry continues throughout ontogeny: Type VI allometric shift).     

Similarity of mammalian body size across the taxonomic hierarchy and across space and time

Although it is commonly assumed that closely related animals are similar in body size, the degree of similarity has not been examined across the taxonomic hierarchy. Moreover, little is known about the variation or consistency of body size patterns across geographic space or evolutionary time. Here, we draw from a data set of terrestrial, nonvolant mammals to quantify and compare patterns across the body size spectrum, the taxonomic hierarchy, continental space, and evolutionary time. We employ a variety of statistical techniques including "sib-sib" regression, phylogenetic autocorrelation, and nested ANOVA. We find an extremely high resemblance (heritability) of size among congeneric species for mammals over approximately 18 g; the result is consistent across the size spectrum. However, there is no significant relationship among the body sizes of congeneric species for mammals under approximately 18 g. We suspect that life-history and ecological parameters are so tightly constrained by allometry at diminutive size that animals can only adapt to novel ecological conditions by modifying body size. The overall distributions of size for each continental fauna and for the most diverse orders are quantitatively similar for North America, South America, and Africa, despite virtually no overlap in species composition. Differences in ordinal composition appear to account for quantitative differences between continents. For most mammalian orders, body size is highly conserved, although there is extensive overlap at all levels of the taxonomic hierarchy. The body size distribution for terrestrial mammals apparently was established early in the Tertiary, and it has remained remarkably constant over the past 50 Ma and across the major continents. Lineages have diversified in size to exploit environmental opportunities but only within limits set by allometric, ecological, and evolutionary constraints.     

Phenotypic integration of the cervical vertebrae in the Hominoidea (Primates)

Phenotypic integration and modularity represent important factors influencing evolutionary change. The mammalian cervical vertebral column is particularly interesting in regards to integration and modularity because it is highly constrained to seven elements, despite widely variable morphology. Previous research has found a common pattern of integration among quadrupedal mammals, but integration patterns also evolve in response to locomotor selective pressures like those associated with hominin bipedalism. Here, I test patterns of covariation in the cervical vertebrae of three hominoid primates (Hylobates, Pan, Homo) who engage in upright postures and locomotion. Patterns of integration in the hominoid cervical vertebrae correspond generally to those previously found in other mammals, suggesting that integration in this region is highly conserved, even among taxa that engage in novel positional behaviors. These integration patterns reflect underlying developmental as well as functional modules. The strong integration between vertebrae suggests that the functional morphology of the cervical vertebral column should be considered as a whole, rather than in individual vertebrae. Taxa that display highly derived morphologies in the cervical vertebrae are likely exploiting these integration patterns, rather than reorganizing them. Future work on vertebrates without cervical vertebral number constraints will further clarify the evolution of integration in this region.