Campbell Rolian

Deciphering the Palimpsest: Studying the Relationship Between Morphological Integration and Phenotypic Covariation

Organisms represent a complex arrangement of anatomical structures and individuated parts that must maintain functional associations through development. This integration of variation between functionally related body parts and the modular organization of development are fundamental determinants of their evolvability. This is because integration results in the expression of coordinated variation that can create preferred directions for evolutionary change, while modularity enables variation in a group of traits or regions to accumulate without deleterious effects on other aspects of the organism. Using our own work on both model systems (e.g., lab mice, avians) and natural populations of rodents and primates, we explore in this paper the relationship between patterns of phenotypic covariation and the developmental determinants of integration that those patterns are assumed to reflect. We show that integration cannot be reliably studied through phenotypic covariance patterns alone and argue that the relationship between phenotypic covariation and integration is obscured in two ways. One is the superimposition of multiple determinants of covariance in complex systems and the other is the dependence of covariation structure on variances in covariance-generating processes. As a consequence, we argue that the direct study of the developmental determinants of integration in model systems is necessary to fully interpret patterns of covariation in natural populations, to link covariation patterns to the processes that generate them, and to understand their significance for evolutionary explanation.

Locomotor anatomy and biomechanics of the Dmanisi hominins

The Dmanisi hominins inhabited a northern temperate habitat in the southern Caucasus, approximately 1.8 million years ago. This is the oldest population of hominins known outside of Africa. Understanding the set of anatomical and behavioral traits that equipped this population to exploit their seasonal habitat successfully may shed light on the selection pressures shaping early members of the genus Homo and the ecological strategies that permitted the expansion of their range outside of the African subtropics. The abundant stone tools at the site, as well as taphonomic evidence for butchery, suggest that the Dmanisi hominins were active hunters or scavengers. In this study, we examine the locomotor mechanics of the Dmanisi hind limb to test the hypothesis that the inclusion of meat in the diet is associated with an increase in walking and running economy and endurance. Using comparative data from modern humans, chimpanzees, and gorillas, as well as other fossil hominins, we show that the Dmanisi hind limb was functionally similar to modern humans, with a longitudinal plantar arch, increased limb length, and human-like ankle morphology. Other aspects of the foot, specifically metatarsal morphology and tibial torsion, are less derived and similar to earlier hominins. These results are consistent with hypotheses linking hunting and scavenging to improved walking and running performance in early Homo. Primitive retentions in the Dmanisi foot suggest that locomotor evolution continued through the early Pleistocene.

Walking, running and the evolution of short toes in humans

SUMMARY The phalangeal portion of the forefoot is extremely short relative to body mass in humans. This derived pedal proportion is thought to have evolved in the context of committed bipedalism, but the benefits of shorter toes for walking and/or running have not been tested previously. Here, we propose a biomechanical model of toe function in bipedal locomotion that suggests that shorter pedal phalanges improve locomotor performance by decreasing digital flexor force production and mechanical work, which might ultimately reduce the metabolic cost of flexor force production during bipedal locomotion. We tested this model using kinematic, force and plantar pressure data collected from a human sample representing normal variation in toe length (N=25). The effect of toe length on peak digital flexor forces, impulses and work outputs was evaluated during barefoot walking and running using partial correlations and multiple regression analysis, controlling for the effects of body mass, whole-foot and phalangeal contact times and toe-out angle. Our results suggest that there is no significant increase in digital flexor output associated with longer toes in walking. In running, however, multiple regression analyses based on the sample suggest that increasing average relative toe length by as little as 20% doubles peak digital flexor impulses and mechanical work, probably also increasing the metabolic cost of generating these forces. The increased mechanical cost associated with long toes in running suggests that modern human forefoot proportions might have been selected for in the context of the evolution of endurance running.

THE COEVOLUTION OF HUMAN HANDS AND FEET

Human hands and feet have longer, more robust first digits, and shorter lateral digits compared to African apes. These similarities are often assumed to be independently evolved adaptations for manipulative activities and bipedalism, respectively. However, hands and feet are serially homologous structures that share virtually identical developmental blueprints, raising the possibility that digital proportions coevolved in human hands and feet because of underlying developmental linkages that increase phenotypic covariation between them. Here we show that phenotypic covariation between serially homologous fingers and toes in Homo and Pan is not only higher than expected, it also causes these digits to evolve along highly parallel trajectories under episodes of simulated directional selection, even when selection pressures push their means in divergent directions. Further, our estimates of the selection pressures required to produce human‐like fingers and toes from an African ape‐like ancestor indicate that selection on the toes was substantially stronger, and likely led to parallel phenotypic changes in the hands. Our data support the hypothesis that human hands and feet coevolved, and suggest that the evolution of long robust big toes and short lateral toes for bipedalism led to changes in hominin fingers that may have facilitated the emergence of stone tool technology.

Integration and Evolvability in Primate Hands and Feet

Morphological integration theory predicts that sets of phenotypic traits that covary strongly due to developmental and/or functional connections between them eventually co-evolve because of a coordinated response to selection, and accordingly become less independently evolvable. This process is not irreversible, however, and phenotypic traits can become less integrated, and hence more independently evolvable, in the context of selection for divergent functions and morphologies. This study examines the reciprocal relationship between shared function, integration and evolvability by comparing integration patterns among serially homologous skeletal elements in the hands and feet of a functionally diverse sample of catarrhine primates. Two hypotheses are tested: (1) species in which the autopods are functionally more similar (e.g. quadrupedal monkeys) have more strongly integrated autopods than species in which the autopods are functionally divergent (e.g. gibbons, humans) and (2) the latter have autopods that are more evolvable, collectively and independently. Morphometric data from selected hand and foot digital rays were used to derive phenotypic variance/covariance matrices. The strength of integration among autopods was quantified using eigenanalysis and a measure of trait variational autonomy. Evolvability was estimated by subjecting phenotypic variance/covariance matrices to simulated random selection gradients, and comparing evolutionary responses among species. Results indicate that integration decreases as hands and feet become functionally divergent, and that the strongly integrated hand and foot skeletons of quadrupedal monkeys respond to selection in a highly collinear manner, even when simulated selective pressures acting on each autopod are in opposite directions in phenotypic space. Results confirm that the evolvability of morphological traits depends largely on how strongly they covary with other traits, but also with body size. The role of pleiotropy as a developmental mechanism underlying integration and evolvability is also discussed.

Rediscovering Waddington in the post‐genomic age

Conrad Hal Waddington was a revolutionary interdisciplinary thinker well ahead of his time. Many of his ideas have been subsumed into our current understanding of developmental biology [1]. His pioneering theories, first published in the mid-20th century, continue to find validation 50 years later in the molecular era of developmental genetics [2]. Among his many contributions, Waddington [3] introduced the term epigenetics to describe the full variety of emergent developmental phenomena above the level of the genome, and elegantly expressed these ideas in the form of his widely recognised and explicitly evolutionary epigenetic landscape metaphor [3]. These emergent phenomena bridge the gap between genotype and phenotype, and comprise the epigenotype [5]. Because of this close relationship between development and evolution, it is important to grasp how such epigenetic mechanisms function. The diverse use of the term epigenetics in the subsequent literature has led to substantial disagreement about what exactly is being discussed, and at which level(s) of inquiry, despite several attempts to achieve consensus [6, 7]. In most contemporary biological contexts, epigenetics refers to chromatin modification [8]. Not only does Waddington’s more inclusive definition appear to have been largely abandoned, also the different uses of his term have coincided with the near disappearance of the original concept of epigenetics from models of evolutionary change [9]. We see this as a potentially significant problem for evolutionary biologists. In this essay our focus is on the theoretical concepts originally specified by Waddington’s epigenetics. We argue that, in this age of powerful postgenomic laboratory and bioinformatics tools, epigenetics sensu Waddington is more informative and instructive than it has been for decades. Waddington’s epigenetics has the potential to shed new light on the means by which both selectable variation and innovation, two key features of evolutionary theory, are

Digit ratios predict polygyny in early apes, Ardipithecus, Neanderthals and early modern humans but not in Australopithecus

Social behaviour of fossil hominoid species is notoriously difficult to predict owing to difficulties in estimating body size dimorphism from fragmentary remains and, in hominins, low canine size dimorphism. Recent studies have shown that the second-to-fourth digit ratio (2D : 4D), a putative biomarker for prenatal androgen effects (PAEs), covaries with intra-sexual competition and social systems across haplorrhines; non-pair-bonded polygynous taxa have significantly lower 2D : 4D ratios (high PAE) than pair-bonded monogamous species. Here, we use proximal phalanx ratios of extant and fossil specimens to reconstruct the social systems of extinct hominoids. Pierolapithecus catalaunicus, Hispanopithecus laietanus and Ardipithecus ramidus have ratios consistent with polygynous extant species, whereas the ratio of Australopithecus afarensis is consistent with monogamous extant species. The early anatomically modern human Qafzeh 9 and Neanderthals have lower digit ratios than most contemporary human populations, indicating increased androgenization and possibly higher incidence of polygyny. Although speculative owing to small sample sizes, these results suggest that digit ratios represent a supplementary approach for elucidating the social systems of fossil hominins.

The Developmental Basis of Quantitative Craniofacial Variation in Humans and Mice

The human skull is a complex and highly integrated structure that has long held the fascination of anthropologists and evolutionary biologists. Recent studies of the genetics of craniofacial variation reveal a very complex and multifactorial picture. These findings contrast with older ideas that posit much simpler developmental bases for variation in cranial morphology such as the growth of the brain or the growth of the chondrocranium relative to the dermatocranium. Such processes have been shown to have major effects on cranial morphology in mice. It is not known, however, whether they are relevant to explaining normal phenotypic variation in humans. To answer this question, we obtained vectors of shape change from mutant mouse models in which the developmental basis for the craniofacial phenotype is known to varying degrees, and compared these to a homologous dataset constructed from human crania obtained from a single population with a known genealogy. Our results show that the shape vectors associated with perturbations to chondrocranial growth, brain growth, and body size in mice do largely correspond to axes of covariation in humans. This finding supports the view that the developmental basis for craniofacial variation funnels down to a relatively small number of key developmental processes that are similar across mice and humans. Understanding these processes and how they influence craniofacial shape provides fundamental insights into the developmental basis for evolutionary change in the human skull as well as the developmental-genetic basis for normal phenotypic variation in craniofacial form.

An assessment of orofacial clefts in Tanzania

BackgroundClefts of the lip (CL), the palate (CP), or both (CLP) are the most common orofacial congenital malformations found among live births, accounting for 65% of all head and neck anomalies. The frequency and pattern of orofacial clefts in different parts of the world and among different human groups varies widely. Generally, populations of Asian or Native American origin have the highest prevalence, while Caucasian populations show intermediate prevalence and African populations the lowest. To date, little is known regarding the epidemiology and pattern of orofacial clefts in Tanzania.MethodsA retrospective descriptive study was conducted at Bugando Medical Centre to identify all children with orofacial clefts that attended or were treated during a period of five years. Cleft lip and/or palate records were obtained from patient files in the Hospitals Departments of Surgery, Paediatrics and medical records. Age at presentation, sex, region of origin, type and laterality of the cleft were recorded. In addition, presence of associated congenital anomalies or syndromes was recorded.ResultsA total of 240 orofacial cleft cases were seen during this period. Isolated cleft lip was the most common cleft type followed closely by cleft lip and palate (CLP). This is a departure from the pattern of clefting reported for Caucasian and Asian populations, where CLP or isolated cleft palate is the most common type. The distribution of clefts by side showed a statistically significant preponderance of the left side (43.7%) (χ2 = 92.4, p < 0.001), followed by the right (28.8%) and bilateral sides (18.3%). Patients with isolated cleft palate presented at very early age (mean age 1.00 years, SE 0.56). Associated congenital anomalies were observed in 2.8% of all patients with orofacial clefts, and included neural tube defects, Talipes and persistent ductus arteriosus.ConclusionsUnilateral orofacial clefts were significantly more common than bilateral clefts; with the left side being the most common affected side. Most of the other findings did not show marked differences with orofacial cleft distributions in other African populations.

Reassessing manual proportions in Australopithecus afarensis

Previous analyses of hand morphology in Australopithecus afarensis have concluded that this taxon had modern human-like manual proportions, with relatively long thumbs and short fingers. These conclusions are based on the A.L.333 composite fossil assemblage from Hadar, Ethiopia, and are premised on the ability to assign phalanges to a single individual, and to the correct side and digit. Neither assignment is secure, however, given the taphonomy and sample composition at A.L.333. We use a resampling approach that includes the entire assemblage of complete hand elements at Hadar, and takes into account uncertainties in identifying phalanges by individual, side and digit number. This approach provides the most conservative estimates of manual proportions in Au. afarensis. We resampled hand long bone lengths in Au. afarensis and extant hominoids, and obtained confidence limits for distributions of manual proportions in the latter. Results confirm that intrinsic manual proportions in Au. afarensis are dissimilar to Pan and Pongo. However, manual proportions in Au. afarensis often fall at the upper end of the distribution in Gorilla, and very lower end in Homo, corresponding to disproportionately short thumbs and long medial digits in Homo. This suggests that manual proportions in Au. afarensis, particularly metacarpal proportions, were not as derived towards Homo as previously described, but rather are intermediate between gorillas and humans. Functionally, these results suggest Au. afarensis could not produce precision grips with the same efficiency as modern humans, which may in part account for the absence of lithic technology in this fossil taxon.