Christophe Soligo

Using the fossil record to estimate the age of the last common ancestor of extant primates

Divergence times estimated from molecular data often considerably predate the earliest known fossil representatives of the groups studied. For the order Primates, molecular data calibrated with various external fossil dates uniformly suggest a mid-Cretaceous divergence from other placental mammals, some 90 million years (Myr) ago, whereas the oldest known fossil primates are from the basal Eocene epoch (54–55 Myr ago). The common ancestor of primates should be earlier than the oldest known fossils, but adequate quantification is needed to interpret possible discrepancies between molecular and palaeontological estimates. Here we present a new statistical method, based on an estimate of species preservation derived from a model of the diversification pattern, that suggests a Cretaceous last common ancestor of primates, approximately 81.5 Myr ago, close to the initial divergence time inferred from molecular data. It also suggests that no more than 7% of all primate species that have ever existed are known from fossils. The approach unites all the available palaeontological methods of timing evolutionary events: the fossil record, extant species and clade diversification models.

Dating Primate Divergences through an Integrated Analysis of Palaeontological and Molecular Data

Estimation of divergence times is usually done using either the fossil record or sequence data from modern species. We provide an integrated analysis of palaeontological and molecular data to give estimates of primate divergence times that utilize both sources of information. The number of preserved primate species discovered in the fossil record, along with their geological age distribution, is combined with the number of extant primate species to provide initial estimates of the primate and anthropoid divergence times. This is done by using a stochastic forwards-modeling approach where speciation and fossil preservation and discovery are simulated forward in time. We use the posterior distribution from the fossil analysis as a prior distribution on node ages in a molecular analysis. Sequence data from two genomic regions (CFTR on human chromosome 7 and the CYP7A1 region on chromosome 8) from 15 primate species are used with the birth-death model implemented in mcmctree in PAML to infer the posterior distribution of the ages of 14 nodes in the primate tree. We find that these age estimates are older than previously reported dates for all but one of these nodes. To perform the inference, a new approximate Bayesian computation (ABC) algorithm is introduced, where the structure of the model can be exploited in an ABC-within-Gibbs algorithm to provide a more efficient analysis.

The macroevolutionary consequences of phenotypic integration: From development to deep time

Phenotypic integration is a pervasive characteristic of organisms. Numerous analyses have demonstrated that patterns of phenotypic integration are conserved across large clades, but that significant variation also exists. For example, heterochronic shifts related to different mammalian reproductive strategies are reflected in postcranial skeletal integration and in coordination of bone ossification. Phenotypic integration and modularity have been hypothesized to shape morphological evolution, and we extended simulations to confirm that trait integration can influence both the trajectory and magnitude of response to selection. We further demonstrate that phenotypic integration can produce both more and less disparate organisms than would be expected under random walk models by repartitioning variance in preferred directions. This effect can also be expected to favour homoplasy and convergent evolution. New empirical analyses of the carnivoran cranium show that rates of evolution, in contrast, are not strongly influenced by phenotypic integration and show little relationship to morphological disparity, suggesting that phenotypic integration may shape the direction of evolutionary change, but not necessarily the speed of it. Nonetheless, phenotypic integration is problematic for morphological clocks and should be incorporated more widely into models that seek to accurately reconstruct both trait and organismal evolution.

Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution

Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.

Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates

Variation in relative brain size is commonly interpreted as the result of selection on neuronal capacity. However, this approach ignores that relative brain size is also linked to another highly adaptive variable: body size. Considering that one-way tradeoff mechanisms are unlikely to provide satisfactory evolutionary explanations, we introduce an analytical framework that describes and quantifies all possible evolutionary scenarios between two traits. To investigate the effects of body mass changes on the interpretation of relative brain size evolution, we analyze three mammalian orders that are expected to be subject to different selective pressures on body size due to differences in locomotor adaptation: bats (powered flight), primates (primarily arboreal), and carnivorans (primarily terrestrial). We quantify rates of brain and body mass changes along individual branches of phylogenetic trees using an adaptive peak model of evolution. We find that the magnitude and variance of the level of integration of brain and body mass rates, and the subsequent relative influence of either brain or body size evolution on the brain–body relationship, differ significantly between orders and subgroups within orders. Importantly, we find that variation in brain–body relationships was driven primarily by variability in body mass. Our approach allows a more detailed interpretation of correlated trait evolution and variation in the underlying evolutionary pathways. Results demonstrate that a principal focus on interpreting relative brain size evolution as selection on neuronal capacity confounds the effects of body mass changes, thereby hiding important aspects that may contribute to explaining animal diversity.

Primate Origins: Implications of a Cretaceous Ancestry

It has long been accepted that the adaptive radiation of modern placental mammals, like that of modern birds, did not begin until after the Cretaceous/Tertiary (K/T) boundary 65 million years (Ma) ago, following the extinction of the dinosaurs. The first undoubted fossil relatives of modern primates appear in the record 55 Ma ago. However, in agreement with evidence from molecular phylogenies calibrated with dates from denser parts of the fossil record, a statistical analysis of the primate record allowing for major gaps now indicates a Cretaceous origin of euprimates 80–90 Ma ago. If this interpretation is correct, primates overlapped with dinosaurs by some 20 Ma prior to the K/T boundary, and the initial radiation of primates was probably truncated as part of the major extinction event that occurred at the end of the Cretaceous. Following a review of evidence for an early origin of primates, implications of this are discussed with respect to the likely ancestral condition for primates, including a southern continental area of origin and moderately large body size. The known early Tertiary primates are re-interpreted as northern continental offshoots of a ‘second wave’ of primate evolution.

Anatomy of the hand and arm in Daubentonia madagascariensis : A functional and phylogenetic outlook

The aye-aye (Daubentonia madagascariensis) is easily the most enigmatic of living primates. It sports a unique combination of derived characters, including continuously growing incisors, functional claws, the largest hand of any primate and a highly modified middle finger. The specialised middle finger is no longer used in locomotion and serves as a probe-like instrument for investigating, locating and extracting xylophagous (wood-boring) larvae as well as other food items. Its phalanges can be moved both at great speed and independently of each other. The present study reports on dissections of the forelimbs of two individuals of D. madagascariensis and one specimen each of Lemur catta and Cercopithecus cephus. Derived characters of the forelimb musculature in Daubentonia are interpreted within the context of its distinct locomotor and foraging adaptations. The primary adaptations underlying speed and mobility in the third manual digit of Daubentonia are found in the intrinsic hand musculature and notably in the arrangement of the dorsal aponeurosis. Implications for the interpretation of suggested convergences between the aye-aye, the diprotodont marsupial Dactylopsila palpator and the early Tertiary apatemyid genus Heterohyus are discussed.

Inter‐ and intra‐specific scaling of articular surface areas in the hominoid talus

The morphology of postcranial articular surfaces is expected to reflect their weight‐bearing properties, as well as the stability and mobility of the articulations to which they contribute. Previous studies have mainly confirmed earlier predictions of isometric scaling between articular surface areas and body mass; the exception to this is ‘male‐type’, convex articular surface areas, which may scale allometrically due to differences in locomotor strategies within the analysed samples. In the present study, we used new surface scanning technology to quantify more accurately articular surface areas and to test those predictions within the talus of hominoid primates, including modern humans. Our results, contrary to predictions, suggest that there are no generalised rules of articular scaling within the talus of hominoids. Instead, we suggest that articular scaling patterns are highly context‐specific, depending on the role of each articulation during locomotion, as well as taxon‐ and sex‐specific differences in locomotion and ontogenetic growth trajectories within any given sample. While this may prove problematic for inferring body mass based on articular surface area, it also offers new opportunities of gaining substantial insights into the locomotor patterns of extinct species.

New Light on the Dates of Primate Origins and Divergence

The known fossil record for undoubted primates of modern aspect (i.e., confined to Euprimates and excluding Plesiadapiformes) dates back to the beginning of the Eocene epoch, about 55 million years ago (MYA), and it is widely accepted among primate paleontologists that primates originated during the preceding Paleocene epoch, some 60–65 MYA. A parallel conclusion has been reached for most orders of placental mammals, and it is generally assumed that the origin and radiation of most if not all placental orders with extant representatives took place after the extinction of dinosaurs at the end of the Cretaceous. In common parlance, the Age of Mammals followed on from the Age of Dinosaurs. A comparable explanation has been given for the adaptive radiation of modern birds. All such interpretations depend on the

Sexual dimorphism and laterality in the evolution of the primate prefrontal cortex.

Social selective pressures are commonly considered as the main driving force of primate brain evolution. Primate social behaviour is, however, known to be sexually dimorphic, and no previous study has made a direct comparison between male and female brain structures across species. We quantify sex-specific evolutionary trends in the prefrontal cortex of anthropoid primates (including humans) to investigate how sexual selection has shaped brain evolution in primates. The prefrontal cortex is of particular importance to the investigation of sexual dimorphism in primate brain evolution because of its association to those cognitive capacities central to primate (and human) evolution: sociality and higher-order cognitive processing. Our results demonstrate sex-by-hemisphere differences in the evolution of the prefrontal cortex in humans and non-human anthropoid primates congruent with the principal selective pressures considered to underlie anthropoid behavioural evolution. Our findings further show how sexual selection can shape brain adaptation in primates and provide an evolutionary framework for interpreting sex and sex-by-hemisphere differences in cortical organization in humans and non-human primates.