Macroevolutionary analysis of Primates with special reference to the genus Homo

The present thesis focusses on fossil Primates, their ecological characterization, morphological evolution and diversification, and an array of new tools to study their anatomical features. The text is divided in three different parts, presenting a collection of either published or submitted manuscripts. The first part regards the morphological adaptation and diversification of Primates. The inaugural paper (“Macroevolutionary trends of brain size in primates”, Melchionna et al., under review) deals with the identification and the analysis of macroevolutionary trends in brain size evolution in Primates. We applied Phylogenetic Ridge Regression (RRphylo) to found possible shifts in morphological rates and their temporal trend. Furthermore, we computed diversification rates (DR). We found a significant increase in encephalization quotient (EQ) rates in the hominins group with an overall increase in EQ values. We found a significant correlation between DR and both EQ rates EQ values. There is also a linear relationship between speciation and extinction rates. Eventually, we found an increase in speciation rates and a reduction in extinction rates with an increase in EQ values. The second paper (“Unexpectedly rapid evolution of mandibular shape in hominins”; Raia et al., 2018) is about the evolution of mandibular shape from ancient primates to the genus Homo. We used the Geometric Mophometrics and the Phylogenetic Ridge Regression to compute evolutionary rates in mandibular morphology. We found that mandible shape evolution in hominins is exceptionally rapid as compared to any other primate clade. In the second part of the thesis I introduce new advances in the field of the Virtual Anthropology. The first is a new protocol to obtain three-dimensional reconstruction of inner and outer surfaces of fossil specimens (“Reproducing the internal and external anatomy of fossil bones: Two new automatic digital tools”; Profico et al., 2018). By using the R software platform, we developed two automatic tools to reproduce the internal and external structures of bony elements. The first method, Computer‐Aided Laser Scanner Emulator (CA‐LSE), provides the reconstruction of the external portions of a 3D mesh by simulating the action of a laser scanner. The second method, Automatic Segmentation Tool for 3D objects (AST‐3D), performs the digital reconstruction of anatomical cavities. Both methods are embedded in the packages “Arothron” (Profico et al., 2018) and "Morpho" (Schlager, 2017). The second protocol presented in this section is about the reconstruction of the original shape of fossil bones damaged and deformed by taphonomical processes (“A new tool for digital alignment in Virtual Anthropology”; Profico et al., 2018). We developed a new, semi-automatic alignment R software, Digital Tool for Alignment (DTA). This tool uses the shape information contained in a reference sample to find the best alignment solution for the disarticulated regions. The third part of the thesis focusses on Homo, and in particularl on the relationship between Homo neanerthalesis and Homo sapiens. The first paper of this section is about the status of the Neanderthal niche fragmentation toward their demise (“Fragmentation of Neanderthals' pre-extinction distribution by climate change”; Melchionna et al., 2018). By using Species Distribution Models, and a habitat fragmentation analysis, we reconstructed the ecological niche of both human species. We found Homo sapiens had greater ecological plasticity over Neanderthals, which probably allowed this species to better react to climatic worsening at 44 and then at 40 ka. However, Neanderthals potential habitat appears to be very reduced and fragmented during the last phase of their occupation. The second paper of this last section regards the role of Homo sapiens in the Late Pleistocene megafauna extinction (“The well-behaved killer: Late Pleistocene humans in Eurasia were significantly associated with living megafauna only”; Carotenuto et al., 2018). Starting from a rich faunal and archaeological database, and by using SDMs, we obtained megafauna and humans occurrence probability maps over the last 40 ka in Eurasia. Then, we divided species in ecological groups (i.e., body size and feeding category combined). We evaluated their geographical overlap to human range and the species suitability in the core area of Homo sapiens. The results indicated that the extinct megafauna was rare within humans' range and Palaeolithic hunters had stronger association to extant rather than extinct herbivorous species

Arothron: An R package for geometric morphometric methods and virtual anthropology applications

Objectives The statistical analysis of fossil remains is essential to understand the evolution of the genus Homo. Unfortunately, the human fossil record is straight away scarce and plagued with severe loss of information caused by taphonomic processes. The recently developed field of Virtual Anthropology helps to ameliorate this situation by using digital techniques to restore damaged and incomplete fossils. Materials and methods We present the package Arothron, an R software suite meant to process and analyze digital models of skeletal elements. Arothron includes tools to digitally extract virtual cavities such as cranial endocasts, to statistically align disarticulated or broken bony elements, and to visualize local variations between surface meshes and landmark configurations. Results We describe the main functionalities of Arothron and illustrate their usage through reproducible case studies. We describe a tool for segmentation of skeletal cavities by showing its application on a malleus bone, a Neanderthal tooth, and a modern human cranium, reproducing their shape and calculating their volume. We illustrate how to digitally align a disarticulated model of a modern human cranium, and how to combine piecemeal shape information on individual specimens into one. In addition, we present useful visualization tools by comparing the morphological differences between the right hemisphere of the Neanderthal and the modern human brain. Conclusions The Arothron R package is designed to study digital models of fossil specimens. By using Arothron, scientists can handle digital models with ease, investigate the inner morphology of 3D skeletal models, gain a full representation of the original shapes of damaged specimens, and compare shapes across specimens

Testing for changes in rate of evolution and position of the climatic niche of clades

1. There is solid recognition that phylogenetic effects must be acknowledged to appreciate climatic niche variability among species clades properly. Yet, most currently available methods either work at the intra- specific level (hence they ignore phylogeny) or rely on the Brownian motion model of evolution to estimate phylogenetic effects on climatic niche variation. The Brownian mo-tion model may be inappropriate to describe niche evolution in several cases, and even a significant phylogenetic signal in climatic variables does not in-dicate that the effect of shared ancestry was relevant to niche evolution.2. We introduce a new phylogenetic comparative method which describes sig-nificant changes in the width and position of the climatic niche at the inter-specific (clade) level, while making no a priori assumption about how niche evolution took place.3. We devised the R function phylo.niche.shift to estimate whether the climatic niches of individual clades in the tree are either wider or narrower than expected, and whether the niche occupies unexpected climates. We tested phylo.niche.shift on realistic virtual species’ distribution patterns applied to a phylogeny of 365 extant primate species.4. We demonstrate via simulations that the new method is fast and accurate under widely different climatic niche evolution scenarios. phylo.niche.shift showed that the capuchin monkeys and langurs occupy much wider, and prosimian much narrower, climatic niche space than expected by their phylogenetic positions.5. phylo.niche.shift may help to improve research on niche evolution by allow-ing researchers to test specific hypotheses on the factors affecting clades’ realised niche width and position, and the potential effects of climate change on species’ distribution

Target Deformation of the Equus stenonis Holotype Skull : A Virtual Reconstruction

Equus stenonis is one of the most prevalent European Pleistocene fossil horses. It is believed to be the possible ancestor of all Old World Early Pleistocene Equus, extant zebras and asses, and as such provides insights into Equus evolution and its biogeography and paleoecology. The Equus stenonis holotype skull (IGF560) was first described by Igino Cocchi in 1867, from the Early Pleistocene locality of Terranuova (Upper Valdarno basin, Italy). IGF560 is a nearly complete, although medio-laterally crushed and badly compressed skull. Here we provide the first application of a new virtual reconstruction protocol, termed Target Deformation, to the Equus stenonis holotype. The protocol extends beyond classic retrodeformation by using target specimens as a guide for the virtual reconstruction. The targets used as a reference are two fragmentary, yet well-preserved E. stenonis skulls, coming from Olivola (Italy; IGF11023) and Dmanisi (Georgia; Dm 5/154.3/4.A4.5), both Early Pleistocene in age. These two specimens do not display any major deformation, but preserve different, only slightly overlapping portions of the skull. The virtual reconstruction protocol we carried out has shown its feasibility, by producing two 3D models whose final morphology is perfectly congruent with the natural variability of a comparative sample of E. stenonis specimens. This study shows the potential of using even broken or otherwise fragmentary specimens to guide retrodeformation in badly distorted and damaged specimens. The application of Target Deformation will allow us to increase the availability of comparative specimens in studies of fossil species morphology and evolution, as well as to the study of taphonomic processes

Seeing the wood through the trees. Combining shape information from different landmark configurations

The geometric morphometric (GM) analysis of complex anatomical structures is an ever more powerful tool to study biological variability, adaptation and evolution. Here, we propose a new method (combinland), developed in R, meant to combine the morphological information contained in different landmark coordinate sets into a single dataset, under a GM context. combinland builds a common ordination space taking into account the entire shape information encoded in the starting configurations. We applied combinland to a Primate case study including 133 skulls belonging to 14 species. On each specimen, we simulated photo acquisitions converting the 3D landmark sets into six 2D configurations along standard anatomical views. The application of combinland shows statistically negligible differences in the ordination space compared to that of the original 3D objects, in contrast to a previous method meant to address the same issue. Hence, we argue combinland allows to correctly retrieve 3D-quality statistical information from 2D landmark configurations. This makes combinland a viable alternative when the extraction of 3D models is not possible, recommended, or too expensive, and to make full use of disparate sources (and views) of morphological information regarding the same specimens. The code and examples for the application of combinland are available in the Arothron R package

A new, fast method to search for morphological convergence with shape data

Morphological convergence is an intensely studied macroevolutionary phenomenon. It refers to the morphological resemblance between phylogenetically distant taxa. Currently available methods to explore evolutionary convergence either: rely on the analysis of the phenotypic resemblance between sister clades as compared to their ancestor, fit different evolutionary regimes to different parts of the tree to see whether the same regime explains phenotypic evolution in phylogenetically distant clades, or assess deviations from the congruence between phylogenetic and phenotypic distances. We introduce a new test for morphological convergence working directly with non-ultrametric (i.e. paleontological) as well as ultrametric phylogenies and multivariate data. The method (developed as the function search.conv within the R package RRphylo) tests whether unrelated clades are morphologically more similar to each other than expected by their phylogenetic distance. It additionally permits using known phenotypes as the most recent common ancestors of clades, taking full advantage of fossil information. We assessed the power of search.conv and the incidence of false positives by means of simulations, and then applied it to three well-known and long-discussed cases of (purported) morphological convergence: the evolution of grazing adaptation in the mandible of ungulates with high-crowned molars, the evolution of mandibular shape in sabertooth cats, and the evolution of discrete ecomorphs among anoles of Caribbean islands. The search.conv method was found to be powerful, correctly identifying simulated cases of convergent morphological evolution in 95% of the cases. Type I error rate is as low as 4-6%. We found search.conv is some three orders of magnitude faster than a competing method for testing convergence

From Smart Apes to Human Brain Boxes. A Uniquely Derived Brain Shape in Late Hominins Clade

Modern humans have larger and more globular brains when compared to other primates. Such anatomical features are further reflected in the possession of a moderately asymmetrical brain with the two hemispheres apparently rotated counterclockwise and slid anteroposteriorly on one another, in what is traditionally described as the Yakovlevian torque. Developmental disturbance in human brain asymmetry, or lack thereof, has been linked to several cognitive disorders including schizophrenia and depression. More importantly, the presence of the Yakovlevian torque is often advocated as the exterior manifestation of our unparalleled cognitive abilities. Consequently, studies of brain size and asymmetry in our own lineage indirectly address the question of what, and when, made us humans, trying to trace the emergence of brain asymmetry and expansion of cortical areas back in our Homo antecedents. Here, we tackle this same issue by studying the evolution of human brain size, shape, and asymmetry on a phylogenetic tree including 19 apes and Homo species, inclusive of our fellow ancestors. We found that a significant positive shift in the rate of brain shape evolution pertains to the clade including modern humans, Neanderthals, and Homo heidelbergensis. Although the Yakovlevian torque is well evident in these species and levels of brain asymmetry are correlated to changes in brain shape, further early Homo species possess the torque. Even though a strong allometric component is present in hominoid brain shape variability, this component seems unrelated to asymmetry and to the rate shift we recorded. These results suggest that changes in brain size and asymmetry were not the sole factors behind the fast evolution of brain shape in the most recent Homo species. The emergence of handedness and early manifestations of cultural modernity in the archeological record nicely coincide with the same three species sharing the largest and most rapidly evolving brains among all hominoids

Diversification Rates and the Evolution of Species Range Size Frequency Distribution

The geographic range sizes frequency distribution (RFD) within clades is typically right-skewed with untransformed data, and bell-shaped or slightly left-skewed under the log-transformation. This means that most species within clades occupy diminutive ranges, whereas just a few species are truly widespread. A number of ecological and evolutionary explanations have been proposed to account for this pattern. Among the latter, much attention has been given to the issue of how extinction and speciation probabilities influence RFD. Numerous accounts now convincingly demonstrate that extinction rate decreases with range size, both in living and extinct taxa. The relationship between range size and speciation rate, though, is much less obvious, with either small or large ranged species being proposed to originate more daughter taxa. Herein, we used a large fossil database including twenty-one animal clades and more than 80,000 fossil occurrences distributed over more than 400 million years of marine metazoans (exclusive of vertebrates) evolution, to test the relationship between extinction rate, speciation rate, and range size. As expected, we found that extinction rate almost linearly decreases with range size. In contrast, speciation rate peaks at the large (but not the largest) end of the range size spectrum. This is consistent with the peripheral isolation mode of allopatric speciation being the main mechanism of species origination. The huge variation in phylogeny, fossilization potential, time of fossilization, and the overarching effect of mass extinctions suggest caution must be posed at generalizing our results, as individual clades may deviate significantly from the general pattern

Oxidized Nanocarbons-Tripeptide Supramolecular Hydrogels: Shape Matters!

Short peptide hydrogels are attractive biomaterials but typically suffer from limited mechanical properties. Inclusion of other nanomaterials can serve the dual purpose of hydrogel reinforcement and of conferring additional physicochemical properties (e.g., self-healing, conductivity), as long as they do not hamper peptide self-assembly. In particular, nanocarbons are ideal candidates, and their physicochemical properties have demonstrated great potential in nanocarbon-polymer gel biomaterials for tissue engineering or drug delivery. Recently, increasing interest in supramolecular hydrogels drove research also on their enhancement with nanocarbons. However, little is known on the effect of nanocarbon morphology on the self-assembly of short peptides, which are among the most popular hydrogel building blocks. In this work, three different oxidized nanocarbons (i.e., carbon nanotube or CNT as 1D material, graphene oxide sheet or GO as 2D material, and carbon nanohorn or CNH as 3D material) were evaluated for their effects on the self-assembly of the unprotected tripeptide Leu-DPhe-DPhe at physiological conditions. Supramolecular hydrogels were obtained in all cases, and viscoelastic properties were clearly affected by the nanocarbons, which increased stiffness and resistance to applied stress. Notably, self-healing behavior was observed only in the case of CNTs. Tripeptide\u2013nanotube interaction was noted already in solution prior to self-assembly, with the tripeptide acting as a dispersing agent in phosphate buffer. Experimental and in silico investigation of the interaction between peptide and CNTs suggests that the latter acts as nucleation templates for self-assembly and reassembly. Overall, we provide useful insights for the future design of composite biomaterials with acquired properties

The role of habitat fragmentation in Pleistocene megafauna extinction in Eurasia

The idea that several small, rather than a single large, habitat areas should hold the highest total species richness (the so-called SLOSS debate) brings into question the importance of habitat fragmentation to extinction risk. SLOSS studies are generally addressed over a short time scale, potentially ignoring the long-term dimension of extinction risk. Here, we provide the first long-term evaluation of the role of habitat fragmentation in species extinction, focusing on 22 large mammal species that lived in Eurasia during the last 200 000 years. By combining species distribution models and landscape pattern analysis, we compared temporal dynamics of habitat spatial structure between extinct and extant species, estimating the size, number and degree of the geographical isolation of their suitable habitat patches. Our results evidenced that extinct mammals went through considerable habitat fragmentation during the last glacial period and started to fare worse than extant species from about 50 ka. In particular, our modelling effort constrains the fragmentation of habitats into a narrow time window, from 46 to 36 ka ago, surprisingly coinciding with known extinction dates of several megafauna species. Landscape spatial structure was the second most important driver affecting megafauna extinction risk (ca 38% importance), after body mass (ca 39%) and followed by dietary preferences (ca 20%). Our results indicate a major role played by landscape fragmentation on extinction. Such evidence provides insights on what might likely happen in the future, with climate change, habitat loss and fragmentation acting as the main forces exerting their negative effects on biodiversity