Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships

The phylogenetic relationships of several hominin species remain controversial. Two methodological issues contribute to the uncertainty—use of partial, inconsistent datasets and reliance on phylogenetic methods that are ill-suited to testing competing hypotheses. Here, we report a study designed to overcome these issues. We first compiled a supermatrix of craniodental characters for all widely accepted hominin species. We then took advantage of recently developed Bayesian methods for building trees of serially sampled tips to test among hypotheses that have been put forward in three of the most important current debates in hominin phylogenetics—the relationship between Australopithecus sediba and Homo, the taxonomic status of the Dmanisi hominins, and the place of the so-called hobbit fossils from Flores, Indonesia, in the hominin tree. Based on our results, several published hypotheses can be statistically rejected. For example, the data do not support the claim that Dmanisi hominins and all other early Homo specimens represent a single species, nor that the hobbit fossils are the remains of small-bodied modern humans, one of whom had Down syndrome. More broadly, our study provides a new baseline dataset for future work on hominin phylogeny and illustrates the promise of Bayesian approaches for understanding hominin phylogenetic relationships.     

Shape Ontogeny of the Distal Femur in the Hominidae with Implications for the Evolution of Bipedality

Heterochrony has been invoked to explain differences in the morphology of modern humans as compared to other great apes. The distal femur is one area where heterochrony has been hypothesized to explain morphological differentiation among Plio-Pleistocene hominins. This hypothesis is evaluated here using geometric morphometric data to describe the ontogenetic shape trajectories of extant hominine distal femora and place Plio-Pleistocene hominins within that context. Results of multivariate statistical analyses showed that in both Homo and Gorilla, the shape of the distal femur changes significantly over the course of development, whereas that of Pan changes very little. Development of the distal femur of Homo is characterized by an elongation of the condyles, and a greater degree of enlargement of the medial condyle relative to the lateral condyle, whereas Gorilla are characterized by a greater degree of enlargement of the lateral condyle, relative to the medial. Early Homo and Australopithecus africanus fossils fell on the modern human ontogenetic shape trajectory and were most similar to either adult or adolescent modern humans while specimens of Australopithecus afarensis were more similar to Gorilla/Pan. These results indicate that shape differences among the distal femora of Plio-Pleistocene hominins and humans cannot be accounted for by heterochrony alone; heterochrony could explain a transition from the distal femoral shape of early Homo/A. africanus to modern Homo, but not a transition from A. afarensis to Homo. That change could be the result of genetic or epigenetic factors.     

Disproportionate Cochlear Length in Genus Homo Shows a High Phylogenetic Signal during Apes’ Hearing Evolution

Changes in lifestyles and body weight affected mammal life-history evolution but little is known about how they shaped species’ sensory systems. Since auditory sensitivity impacts communication tasks and environmental acoustic awareness, it may have represented a deciding factor during mammal evolution, including apes. Here, we statistically measure the influence of phylogeny and allometry on the variation of five cochlear morphological features associated with hearing capacities across 22 living and 5 fossil catarrhine species. We find high phylogenetic signals for absolute and relative cochlear length only. Comparisons between fossil cochleae and reconstructed ape ancestral morphotypes show that Australopithecus absolute and relative cochlear lengths are explicable by phylogeny and concordant with the hypothetized ((Pan,Homo),Gorilla) and (Pan,Homo) most recent common ancestors. Conversely, deviations of the Paranthropus oval window area from these most recent common ancestors are not explicable by phylogeny and body weight alone, but suggest instead rapid evolutionary changes (directional selection) of its hearing organ. Premodern (Homo erectus) and modern human cochleae set apart from living non-human catarrhines and australopiths. They show cochlear relative lengths and oval window areas larger than expected for their body mass, two features corresponding to increased low-frequency sensitivity more recent than 2 million years ago. The uniqueness of the “hypertrophied” cochlea in the genus Homo (as opposed to the australopiths) and the significantly high phylogenetic signal of this organ among apes indicate its usefulness to identify homologies and monophyletic groups in the hominid fossil record.     

Evidence of Natural Selection Acting on a Polymorphic Hybrid Incompatibility Locus in Mimulus

As a common cause of reproductive isolation in diverse taxa, hybrid incompatibilities are fundamentally important to speciation. A key question is which evolutionary forces drive the initial substitutions within species that lead to hybrid dysfunction. Previously, we discovered a simple genetic incompatibility that causes nearly complete male sterility and partial female sterility in hybrids between the two closely related yellow monkeyflower species Mimulus guttatus and M. nasutus. In this report, we fine map the two major incompatibility loci—hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2)—to small nuclear genomic regions (each <70 kb) that include strong candidate genes. With this improved genetic resolution, we also investigate the evolutionary dynamics of hms1 in a natural population of M. guttatus known to be polymorphic at this locus. Using classical genetic crosses and population genomics, we show that a 320-kb region containing the hms1 incompatibility allele has risen to intermediate frequency in this population by strong natural selection. This finding provides direct evidence that natural selection within plant species can lead to hybrid dysfunction between species.     

Trabecular Evidence for a Human-Like Gait in Australopithecus africanus

Although the earliest known hominins were apparently upright bipeds, there has been mixed evidence whether particular species of hominins including those in the genus Australopithecus walked with relatively extended hips, knees and ankles like modern humans, or with more flexed lower limb joints like apes when bipedal. Here we demonstrate in chimpanzees and humans a highly predictable and sensitive relationship between the orientation of the ankle joint during loading and the principal orientation of trabecular bone struts in the distal tibia that function to withstand compressive forces within the joint. Analyses of the orientation of these struts using microCT scans in a sample of fossil tibiae from the site of Sterkfontein, of which two are assigned to Australopithecus africanus, indicate that these hominins primarily loaded their ankles in a relatively extended posture like modern humans and unlike chimpanzees. In other respects, however, trabecular properties in Au africanus are distinctive, with values that mostly fall between those of chimpanzees and humans. These results indicate that Au. africanus, like Homo, walked with an efficient, extended lower limb.     

Stress-induced mutagenesis and complex adaptation

Because mutations are mostly deleterious, mutation rates should be reduced by natural selection. However, mutations also provide the raw material for adaptation. Therefore, evolutionary theory suggests that the mutation rate must balance between adaptability—the ability to adapt—and adaptedness—the ability to remain adapted. We model an asexual population crossing a fitness valley and analyse the rate of complex adaptation with and without stress-induced mutagenesis (SIM)—the increase of mutation rates in response to stress or maladaptation. We show that SIM increases the rate of complex adaptation without reducing the population mean fitness, thus breaking the evolutionary trade-off between adaptability and adaptedness. Our theoretical results support the hypothesis that SIM promotes adaptation and provide quantitative predictions of the rate of complex adaptation with different mutational strategies.     

The mid-face of lower Pleistocene hominins and its bearing on the attribution of SK 847 and StW 53

SK 847 and StW 53 have often been cited as evidence for early Homo in South Africa. To examine whether midfacial morphology is in agreement with these attributions, we analyze Euclidean distances calculated from 3-D coordinates on the maxillae of SK 847 and StW 53, as well as Australopithecus africanus (Sts 5, Sts 71), Paranthropus robustus (SK 46, SK 48, SK 52, SK 83), early Homo (KNM-ER 1813, KNM-ER 1805, KNM-ER 3733, KNM-WT 15000), P. boisei (KNM-ER 406, KNM-WT 17000, KNM-WT 17400), Gorilla gorilla (n = 116), Homo sapiens (n = 342), Pan paniscus (n = 21) and P. troglodytes (n = 65). Multivariate analyses separate extant hominoids suggesting we have captured taxonomic affinity. With the exception of SK 847 and SK 52, South African fossils tend to cluster together. P. robustus differs substantially from East African robust megadonts. SK 847 and StW 53 resemble the East African Homo specimens that are the most australopith-like, such as KNM-WT 15000 and KNM-ER 1813. The resemblance between StW 53 and Homo is driven partly by similarities in maxillary size. When distances are scaled, StW 53 aligns with A. africanus, while SK 847 clusters primarily with early Homo.     

Heritability and Evolutionary Potential in Thermal Tolerance Traits in the Invasive Mediterranean Cryptic Species of Bemisia tabaci (Hemiptera: Aleyrodidae)

With advancing global climate change, the analysis of thermal tolerance and evolutionary potential is important in explaining the ecological adaptation and changes in the distribution of invasive species. To reveal the variation of heat resistance and evolutionary potential in the invasive Mediterranean cryptic species of Bemisia tabaci, we selected two Chinese populations—one from Harbin, N China, and one from Turpan, S China—that experience substantial heat and cold stress and conducted knockdown tests under static high- and low-temperature conditions. ANOVAs indicated significant effects of populations and sex on heat knockdown time and chill coma recovery time. The narrow-sense heritability (h ²) estimates of heat tolerance based on a parental half-sibling breeding design ranged from 0.47±0.03 to 0.51±0.06, and the estimates of cold tolerance varied from 0.33±0.07 to 0.36±0.06. Additive genetic variances were significantly different from zero for both heat and cold tolerance. These results suggest that invasive B. tabaci Mediterranean cryptic species possesses a strong ability to respond to thermal selection and develops rapid resistance to climate change.     

Femoral neck structure and function in early hominins

All early (Pliocene–Early Pleistocene) hominins exhibit some differences in proximal femoral morphology from modern humans, including a long femoral neck and a low neck‐shaft angle. In addition, australopiths (Au. afarensis, Au. africanus, Au. boisei, Paranthropus boisei), but not early Homo, have an “anteroposteriorly compressed” femoral neck and a small femoral head relative to femoral shaft breadth. Superoinferior asymmetry of cortical bone in the femoral neck has been claimed to be human‐like in australopiths. In this study, we measured superior and inferior cortical thicknesses at the middle and base of the femoral neck using computed tomography in six Au. africanus and two P. robustus specimens. Cortical asymmetry in the fossils is closer overall to that of modern humans than to apes, although many values are intermediate between humans and apes, or even more ape‐like in the midneck. Comparisons of external femoral neck and head dimensions were carried out for a more comprehensive sample of South and East African australopiths (n = 17) and two early Homo specimens. These show that compared with modern humans, femoral neck superoinferior, but not anteroposterior breadth, is larger relative to femoral head breadth in australopiths, but not in early Homo. Both internal and external characteristics of the australopith femoral neck indicate adaptation to relatively increased superoinferior bending loads, compared with both modern humans and early Homo. These observations, and a relatively small femoral head, are consistent with a slightly altered gait pattern in australopiths, involving more lateral deviation of the body center of mass over the stance limb. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

Morphological correlates of the first metacarpal proximal articular surface with manipulative capabilities in apes,humans and South African early hominins

This study quantifies the metacarpal 1 (MC 1) proximal articular surface using three-dimensional morphometrics in extant hominids and fossil hominins (SK 84, cf. Paranthropus robustus/Homo erectus and StW 418, Australopithecus africanus) to understand which characteristics of the proximal metacarpal 1 are potentially correlated with human manipulative abilities and if they can be used in a paleoanthropological setting. A principal components (PC) analysis was used to compare MC 1 proximal articular surface shape and ANOVA and Tukey's HSD post-hoc tests were conducted to determine differences among groups. Homo is significantly different from nonhuman hominids having a less radioulnarly and dorsovolarly curved articular surface. All nonhuman hominids have more curved articular surface with Gorilla showing the most curved joint. Moreover, this study highlights the presence of a radially extended surface in Homo that may be related to the greater thumb abduction in human manipulation activities. Both fossils analyzed show a great ape-like MC 1 proximal articular surface which, associated with recent trabecular and archaeological evidence, may indicate that the ability to make/use stone tools preceded the morphological adaptations associated today with such behavior.     

Diet and hormonal manipulation reveal cryptic genetic variation: implications for the evolution of novel feeding strategies

When experiencing resource competition or abrupt environmental change, animals often must transition rapidly from an ancestral diet to a novel, derived diet. Yet, little is known about the proximate mechanisms that mediate such rapid evolutionary transitions. Here, we investigated the role of diet-induced, cryptic genetic variation in facilitating the evolution of novel resource-use traits that are associated with a new feeding strategy—carnivory—in tadpoles of spadefoot toads (genus Spea). We specifically asked whether such variation in trophic morphology and fitness is present in Scaphiopus couchii, a species that serves as a proxy for ancestral Spea. We also asked whether corticosterone, a vertebrate hormone produced in response to environmental signals, mediates the expression of this variation. Specifically, we compared broad-sense heritabilities of tadpoles fed different diets or treated with exogenous corticosterone, and found that novel diets can expose cryptic genetic variation to selection, and that diet-induced hormones may play a role in revealing this variation. Our results therefore suggest that cryptic genetic variation may have enabled the evolutionary transition to carnivory in Spea tadpoles, and that such variation might generally facilitate rapid evolutionary transitions to novel diets.     

Experimental studies on the origin of cultivated rice

1) Contributions to the origin of cultivated rice made by the author and his colleagues were briefly reviewed under several headlines.—2) Two parallel series of evolution of cultivated species, the Asian form of Oryza perennis to O. sativa and O. breviligulata to O. glaberrima, were pointed out compared.—3) In both the two series, a continuous array of intergrades between wild and cultivated species is found in a particular region. The pattern of character variations among those intermediate plants was considered as indicating the evolutionary path, and the monophyletic origin of the Indica and Japonica types of O. sativa was discussed.—4) The conditions of establishment of a weedy form of O. perennis found in India were discussed. It was noticed that cultivation by man in itself works as a selective agent for cultivated types.     

Adaptive responses to cool climate promotes persistence of a non-native lizard

Successful establishment and range expansion of non-native species often require rapid accommodation of novel environments. Here, we use common-garden experiments to demonstrate parallel adaptive evolutionary response to a cool climate in populations of wall lizards (Podarcis muralis) introduced from southern Europe into England. Low soil temperatures in the introduced range delay hatching, which generates directional selection for a shorter incubation period. Non-native lizards from two separate lineages have responded to this selection by retaining their embryos for longer before oviposition—hence reducing the time needed to complete embryogenesis in the nest—and by an increased developmental rate at low temperatures. This divergence mirrors local adaptation across latitudes and altitudes within widely distributed species and suggests that evolutionary responses to climate can be very rapid. When extrapolated to soil temperatures encountered in nests within the introduced range, embryo retention and faster developmental rate result in one to several weeks earlier emergence compared with the ancestral state. We show that this difference translates into substantial survival benefits for offspring. This should promote short- and long-term persistence of non-native populations, and ultimately enable expansion into areas that would be unattainable with incubation duration representative of the native range.     

The brain of Homo habilis: A new level of organization in cerebral evolution

New studies have been made on endocranial casts of Olduvai specimens of Homo habilis. The results have been compared with those on other East African H. habilis and other hominoids. The mean absolute endocranial capacity of H. habilis is appreciably larger than the mean for australopithecine species: on the new estimates, the H. habilis mean is 45·1% greater than the A. africanus mean and 24·8% greater than that of A. boisei. New data for relative brain size, expressed by Jerison's Nc and EQ and Hemmer's CC, strongly confirm that it was with H. habilis that there appeared the remarkable autapomorphy of Homo, disproportionate expansion of the brain. Encephalometric studies reveal marked transverse expansion of the cerebrum, especially the frontal and parieto-occipital parts, in H. habilis and increased bulk of the frontal and parietal lobes, a derived feature of Homo. There is moderate cerebral heightening, but little or no cerebral lengthening. The sulcal and gyral pattern of the lateral part of the frontal lobe of H. habilis differs from those of Australopithecus and resembles the derived pattern of Homo. The inferior parietal lobule is prominently developed—an autapomorphy of Homo. The two major cerebral areas governing spoken language in modern man are well represented in the endocasts of H. habilis, a functionally important autapomorphy of Homo. The pattern of middle meningeal vessels is more complex with more anastomoses than in australopithecines: H. habilis shares this derived feature with later forms of Homo. In all these features, the brain of H. habilis had made major advances, beyond the more ape-like australopithecine brain. With H. habilis, cerebral evolution had progressed beyond the stage of “animal hominids” (Australopithecus spp.) to that of “human hominids” (Homo spp.). In functional capacity, in particular, its possession of a structural marker of the neurological basis of spoken language, H. habilis had attained a new evolutionary level of organization.     

Reciprocal Recurrent Selection Compared to within-Strain Selection for Increasing Rate of Egg Lay of Tribolium under Optimal and Stress Conditions

A replicated comparison of reciprocal recurrent selection (rrs) based on crossbred performance and within strain-selection (wss) based on purebred performance was made in three diverse environments over ten generations for the improvement of a heterotic trait, 4-day virgin egg lay of Tribolium castaneum. A selection intensity of 20% based on performance in either an optimum (33°), a mild stress (38°), or a severe stress (28°) environment was applied uniformly. Periodically, the performance of each population was measured in all three environments to provide both direct and correlated responses.—Heritability of egg lay in the base population ranged from 0.36 ± 0.03 in optimum to 0.26 ± 0.03 in severe stress. Estimates of dominance effects assumed significant proportions in severe stress only. Genetic correlations for egg lay in diverse environments were large and positive (.6 to.8).—Only in severe stress did the rrs response significantly exceed that for wss. Quadratic adjustments fitted to response curves revealed that small initial genetic gains under rrs were followed by significantly increasing rates of gain in late generations of selection. The reverse was true for wss. This and evidence from realized heritabilities and genetic correlations suggested that rrs had utilized both additive and dominance effects, but wss response was limited to additive effects.—These results agree with selection theory in demonstrating that purebred selection is more efficient than crossbred selection in utilizing additive gene effects. The latter method has merit when non-additive effects assume significant proportions, and this is the more probable case for severe stress conditions.     

Statistical tests for detecting positive selection by utilizing high-frequency variants

By comparing the low-, intermediate-, and high-frequency parts of the frequency spectrum, we gain information on the evolutionary forces that influence the pattern of polymorphism in population samples. We emphasize the high-frequency variants on which positive selection and negative (background) selection exhibit different effects. We propose a new estimator of θ (the product of effective population size and neutral mutation rate), θ_L, which is sensitive to the changes in high-frequency variants. The new θ_L allows us to revise Fay and Wu's H-test by normalization. To complement the existing statistics (the H-test and Tajima's D-test), we propose a new test, E, which relies on the difference between θ_L and Watterson's θ_W. We show that this test is most powerful in detecting the recovery phase after the loss of genetic diversity, which includes the postselective sweep phase. The sensitivities of these tests to (or robustness against) background selection and demographic changes are also considered. Overall, D and H in combination can be most effective in detecting positive selection while being insensitive to other perturbations. We thus propose a joint test, referred to as the DH test. Simulations indicate that DH is indeed sensitive primarily to directional selection and no other driving forces.     

Size and shape variation in the proximal femur of Australopithecus africanus

Aside from use as estimates of body mass dimorphism and fore to hind limb joint size comparisons, postcranial elements have not often contributed to assessments of variation in Australopithecus africanus. Meanwhile, cranial, facial, and dental size variation is interpreted to be high or moderately high. Further, the cranial base and face express patterns of structural (shape) variation, which are interpreted by some as evidence for the presence of multiple species. Here, the proximal femur is used to consider postcranial size and shape variation in A. africanus. Original fossils from Makapansgat and Sterkfontein, and samples from Homo, Pan, Gorilla, and Pongo were measured. Size variation was assessed by comparing the A. africanus coefficient of variation to bootstrapped distributions of coefficient of variation samples for each taxon. Shape variation was assessed from isometrically adjusted shape variables. First, the A. africanus standard deviation of log transformed shape variables was compared to bootstrapped distributions of logged standard deviations in each taxon. Second, shape variable based Euclidean distances between fossil pairs were compared to pairwise Euclidean distance distributions in each reference taxon. The degree of size variation in the A. africanus proximal femur is consistent with that of a single species, and is most comparable to Homo and Pan, lower than A. afarensis, and lower than some estimates of cranial and dental variation. Some, but not all, shape variables show more variation in A. africanus than in extant taxa. The degree of shape difference between some fossils exceeds the majority of pairwise differences in the reference taxa. Proximal femoral shape, but not size, variation is consistent with high estimates of A. africanus cranial variation.     

Dental Ontogeny in Pliocene and Early Pleistocene Hominins

Until recently, our understanding of the evolution of human growth and development derived from studies of fossil juveniles that employed extant populations for both age determination and comparison. This circular approach has led to considerable debate about the human-like and ape-like affinities of fossil hominins. Teeth are invaluable for understanding maturation as age at death can be directly assessed from dental microstructure, and dental development has been shown to correlate with life history across primates broadly. We employ non-destructive synchrotron imaging to characterize incremental development, molar emergence, and age at death in more than 20 Australopithecus anamensis, Australopithecus africanus, Paranthropus robustus and South African early Homo juveniles. Long-period line periodicities range from at least 6–12 days (possibly 5–13 days), and do not support the hypothesis that australopiths have lower mean values than extant or fossil Homo. Crown formation times of australopith and early Homo postcanine teeth fall below or at the low end of extant human values; Paranthropus robustus dentitions have the shortest formation times. Pliocene and early Pleistocene hominins show remarkable variation, and previous reports of age at death that employ a narrow range of estimated long-period line periodicities, cuspal enamel thicknesses, or initiation ages are likely to be in error. New chronological ages for SK 62 and StW 151 are several months younger than previous histological estimates, while Sts 24 is more than one year older. Extant human standards overestimate age at death in hominins predating Homo sapiens, and should not be applied to other fossil taxa. We urge caution when inferring life history as aspects of dental development in Pliocene and early Pleistocene fossils are distinct from modern humans and African apes, and recent work has challenged the predictive power of primate-wide associations between hominoid first molar emergence and certain life history variables.     

New Horned Dinosaurs from Utah Provide Evidence for Intracontinental Dinosaur Endemism

Background

During much of the Late Cretaceous, a shallow, epeiric sea divided North America into eastern and western landmasses. The western landmass, known as Laramidia, although diminutive in size, witnessed a major evolutionary radiation of dinosaurs. Other than hadrosaurs (duck-billed dinosaurs), the most common dinosaurs were ceratopsids (large-bodied horned dinosaurs), currently known only from Laramidia and Asia. Remarkably, previous studies have postulated the occurrence of latitudinally arrayed dinosaur “provinces,” or “biomes,” on Laramidia. Yet this hypothesis has been challenged on multiple fronts and has remained poorly tested.

Methodology/Principal Findings

Here we describe two new, co-occurring ceratopsids from the Upper Cretaceous Kaiparowits Formation of Utah that provide the strongest support to date for the dinosaur provincialism hypothesis. Both pertain to the clade of ceratopsids known as Chasmosaurinae, dramatically increasing representation of this group from the southern portion of the Western Interior Basin of North America. Utahceratops gettyi gen. et sp. nov.—characterized by short, rounded, laterally projecting supraorbital horncores and an elongate frill with a deep median embayment—is recovered as the sister taxon to Pentaceratops sternbergii from the late Campanian of New Mexico. Kosmoceratops richardsoni gen. et sp. nov.—characterized by elongate, laterally projecting supraorbital horncores and a short, broad frill adorned with ten well developed hooks—has the most ornate skull of any known dinosaur and is closely allied to Chasmosaurus irvinensis from the late Campanian of Alberta.

Conclusions/Significance

Considered in unison, the phylogenetic, stratigraphic, and biogeographic evidence documents distinct, co-occurring chasmosaurine taxa north and south on the diminutive landmass of Laramidia. The famous Triceratops and all other, more nested chasmosaurines are postulated as descendants of forms previously restricted to the southern portion of Laramidia. Results further suggest the presence of latitudinally arrayed evolutionary centers of endemism within chasmosaurine ceratopsids during the late Campanian, the first documented occurrence of intracontinental endemism within dinosaurs.