3D Photogrammetry of Bat Skulls: Perspectives for Macro-evolutionary Analyses Abstract Photogrammetry (PH) is relatively cheap, easy to use, flexible and portable but its power and limitations have not been fully explored for studies of small animals. Here we assessed the accuracy of PH for the reconstruction of 3D digital models of bat skulls by evaluating its potential for evolutionary morphology studies at interspecific (19 species) level. Its reliability was assessed against the performance of micro CT scan (µCT) and laser scan techniques (LS). We used 3D geometric morphometrics and comparative methods to quantify the amount of size and shape variation due to the scanning technique and assess the strength of the biological signal in relation to both the technique error and phylogenetic uncertainty. We found only minor variation among techniques. Levels of random error (repeatability and procrustes variance) were similar in all techniques and no systematic error was observed (as evidenced from principal component analysis). Similar levels of phylogenetic signal, allometries and correlations with ecological variables (frequency of maximum energy and bite force) were detected among techniques. Phylogenetic uncertainty interacted with technique error but without affecting the biological conclusions driven by the evolutionary analyses. Our study confirms the accuracy of PH for the reconstruction of challenging specimens. These results encourage the use of PH as a reliable and highly accessible tool for the study of macro evolutionary processes of small mammals.

The Inhibitory Cascade Model is Not a Good Predictor of Molar Size Covariation Abstract The inhibitory cascade (IC) model is a widely used evolutionary developmental explanation of among-species differences in relative molar tooth size. The IC model posits that, as molars develop from front to back, the relative strength of activating and inhibiting influences establishes a “ratcheting” mechanism leading to predictable relative molar sizes. Such a constraint on molar covariation would lead to strong variational biases on the evolutionary paths that the molar row can traverse through phenotypic space. These constraints manifest themselves in characteristic patterns of variation among species that loosely match observed macroevolutionary patterns. In this paper, we write out the predictions of the IC model for within-species covariation in molar size in a framework that unifies evolutionary developmental biological and quantitative genetic perspectives on the evolution of complex traits. We then evaluate these predictions about aspects of molar covariation in eight anthropoid primate species. We find that the IC model tends to over-predict aspects of within-species covariation by substantial margins. Only macaques exhibit covariation in and among individual teeth consistent with the IC model, but they do not show signs of the strong evolutionary constraint predicted by the model. Gorillas meet none of the predictions. While we cannot rule out an IC-like process as a contributor, causes of molar size covariation other than those described in the IC model must be major contributors to covariation in molar teeth within populations.

Description and Analysis of Spatial Patterns in Geometric Morphometric Data Abstract The development of techniques for the acquisition of high-resolution 3D images, such as computed tomography and magnetic resonance imaging, has opened new avenues to the study of complex morphologies. Detailed descriptions of internal and external traits can be now obtained, allowing the intensive sampling of surface points. In this paper, we introduce a morphometric and statistical framework, grounded on Procrustes and Procrustes-like techniques as well as standard spatial statistics, to explicitly describe and incorporate the spatial pattern of these surface points into the analyses. We exemplified this approach by analyzing ontogenetic changes in a sample of human brain endocasts and inter-specific differences between primate skulls. An intensive sampling of points on 3D surfaces was performed by automatic techniques and the morphometric variation among specimens was measured by the residuals obtained after the alignment of points. Our results showed that shape changes in both examples are spatially structured. Different results were attained by using methods that incorporate or not the spatial structure in the evaluation of the effect of specific biological factors on shape variation. Particularly, these analyses indicated that the effect of biological factors acting at local scales can be confounded with more systemic factors (by example, the effect of the diet on the facial skeleton) if the spatial structure is not taken into account. Overall, our results suggest that the intensive description of shape differences among structures using densely sampled points on 3D surfaces combined with spatial statistical methods can be used to explore problems not widely addressed in morphological studies.

The Apex Set-Up for the Major Transitions in Individuality Abstract Morphological and functional hierarchies occurring in contemporary biological entities are amalgamated via a small number of progressive key-steps termed as Major Transition in Evolution (MTE) that encompass steps of Major Transition in Individuality (MTI). Literature views MTE/MTI in nature as a sequential increase in complexity, and has contributed insights into the emergence of genuine MTI candidates that actually build higher order individuals from simpler entities and into their specific properties. The theory- By considering a novel MTI trajectory termed the ‘MTI continuum’ (independent of the tree of life that contemplates taxonomic correlations), I found no literature consensus for this continuum’s apex. Next, I consider the properties of biological entities termed as ‘superorganism’ (eusocial insects, humans), also considered as highly-developed MTIs. I classify ‘superorganism’ as being on the level of ‘miscellaneous transitions’ that have not yet developed into real MTIs and that do not meet the ‘individual’ physiognomy. Then I assign the emergence of three new MTI diachronic-classes, the colonial-organisms, chimerism and multi-chimerism, suggesting that they represent highly complex MTIs that belong at the apex of the MTI continuum. These novel MTIs are neither fraternal, nor egalitarian, deprived of ‘kinship’ and ‘fairness’ considerations, yet still generate genuine and distinct libertarian entities. I posit that these MTIs embody the qualities of real units of selection.

Craniofacial Allometry is a Rule in Evolutionary Radiations of Placentals Abstract It has been suggested that larger species of mammals tend to become long-faced when they diverge in size during an evolutionary radiation. However, whether this allometric pattern, reminiscent of ontogenetic changes in skull proportions, is indeed a rule has yet to be thoroughly tested. Using ~ 6000 adult specimens from 14 phylogenetically well separated and ecomorphologically distinctive lineages, 11 orders, and all superorders of the placentals, I tested each group for positive craniofacial allometry (CREA). The evidence supporting CREA is overwhelming, with virtually all analyses showing proportionally longer faces in bigger species. This corroborates previous studies in other groups, consolidates CREA as a pervasive morphological trend in placental evolution and opens important research avenues for connecting micro- and macro-evolution. If found in even more lineages of non-placental mammals, confirmed in birds, and possibly discovered in other tetrapods, CREA could become one of the most general rules of morphological evolution in land vertebrates.

What is It Like to be a Crab? A Complex Network Analysis of Eucaridan Evolution Abstract Eucaridan evolution involved a process starting from a body organization characterized by an elongate and cylindrical cephalothorax, a well-developed abdomen composed of swimming appendages, ending in a tail fan formed by flattened uropods and a telson. This process would lead, ultimately, to a body organization characterized by a shortened and depressed cephalothorax, and a reduced and ventrally folded abdomen. This ultimate process is typically known as carcinization, and is commonly defined as the process of becoming a crab. In this work, the evolution of the superorder Eucarida was studied using complex networks. A new definition of crab and carcinization are given based on the results obtained. A crab is a topological structural closure that determines the formation of a triadic central core. The evolution of the crab implied the formation of a triadic structure with high closeness centrality, formed by the cephalon, the fused thoracomere 1–4 and the carapace, which represented a highly stable hierarchical core deeply buried or enclosed in the topological structure of the network, responsible for the generation of a highly integrated and robust topology. Under this new definition, the representative of the infraorder Anomura used in this work, which is commonly considered as a crab, is not. This network seemed to be characterized by the presence of a quasi-dyadic structure, formed by the cephalon and the carapace, which was not sufficient for generating the topological closure.

Genetic Variation in Metabolic Rate and Correlations with Other Energy Budget Components and Life History in Daphnia magna Abstract Much is known about the genetic variance in certain components of metabolism, most notably resting and maximum metabolic rate. This is in stark contrast to the lack of information on genetic variance in the metabolic rate of individuals that feed and express routine activity, and how this rate correlates with other components of the energy budget or life history traits. Here we quantify genetic variance in metabolic rate (MR) under such conditions, as well as food consumption, juvenile somatic growth rate and age at maturation under ad lib food availability in a set of 10 clones of Daphnia magna from a natural population. Broad sense evolvabilities (0.16–0.56%) were on the same order of magnitude as those typically observed for physiological and life history traits, and suggest that all these traits have the potential to evolve within this population. We did not find support for the previously hypothesized positive genetic correlation between metabolic rate and growth rate. Rather, the patterns of genetic correlations suggest that genetic variance in food consumption is the single most influential trait shaping somatic growth rate, but that additional variance in growth can be explained by considering the joint effect of consumption and MR. The genetic variance in consumption and MR also translated into genetic variance in age at maturation, creating a direct link between these energy budget components and a life history trait with strong fitness effects. Moreover, a weak positive correlation between MR and food consumption suggests the presence of substantial amounts of independent genetic control of these traits, consistent with results obtained using genomic approaches.

Age-Specific Reproductive Investment and Offspring Performance in an Orb-web Spider, Argiope radon Abstract Temporal variation in reproductive investment, e.g. maternal egg provisioning, has a substantial effect on offspring fitness therefore has received great attention by evolutionary biologists. Maternal allocation into egg size and egg content directly influences performance of offspring in many taxa, but spiders have rarely been investigated in this regard. In this study, we investigate the temporal changes in maternal reproductive investment and offspring performance in an orb-web, Argiope radon. A group of male and female spiders were mated randomly in the laboratory. Female spiders were kept under standard condition until they laid egg sacs. For each egg sac, egg sac mass, egg size and egg protein content were measured across all egg sacs. Once the spiderlings emerged, emerging time and toleration to starvation of the spiderlings were recorded. Egg sacs laid early in life were heavier, have larger eggs and offspring emerge sooner than the egg sacs laid by the old females. The spiderlings from the early egg sacs were more likely to emerge, however, these offspring had less toleration to starvation than the egg sacs laid by old females. There was no significant correlation between egg size and egg protein content with offspring performance. The results showed how the female spiders strategically allocate resources to egg sacs and its consequences on the offspring emerging time and toleration to starvation. This study suggests an adaptive maternal reproductive investment strategy which allows the female spiders to gain maximum fitness in each reproductive bout.

The Coral of Life Abstract The Tree of Life (ToL) has been of central importance in the biological sciences, usually understood as a model or a metaphor, and portrayed in various graphical forms to summarize the history of life as a single diagram. If it is seen as a mathematical construct—a rooted graph theoretical tree or, as more recently viewed, a directed network [Network of Life (NoL)]—then its proper visualization is not feasible, for both epistemological and technical reasons. As an overview included in this study demonstrates, published ToLs and NoLs are extremely diverse in appearance and content, and they suffer from inevitable bias towards particular groups, or are restricted to a single major taxon. Metaphorical trees are even less useful for the purpose, because ramification is the only property of botanical trees that may be interpreted in an evolutionary or phylogenetic context. This paper argues that corals, as suggested by Darwin in his early notebooks, are superior to trees as metaphors, and may also be used as mathematical models. A coral diagram is useful for portraying past and present life because it is suitable: (1) to illustrate bifurcations and anastomoses, (2) to depict species richness of taxa proportionately, (3) to show chronology, extinct taxa and major evolutionary innovations, (4) to express taxonomic continuity, (5) to expand particulars due to its self-similarity, and (6) to accommodate a genealogy-based, rank-free classification. This paper is supplemented with a figure, The Coral of Life (CoL), which is, to the author’s knowledge, the first attempt to combine all of the above features in a single diagram for the entirety of life, thus serving as a prototype for further analysis and improvement. The discussion is partly historical: references to classical and modern writings help the reader to understand how biological thinking and methods of visualization have evolved to reach this achievement.

Ecological and Spatial Patterns Associated with Diversification of the Shrub Genus Tetraglochin along Southern-Central Andes (Rosaceae) Abstract In addition to the degree of geographical isolation (sympatry, parapatry, allopatry and peripatry), ecology can be an important factor promoting diversification of lineages, both by niche divergence as well as niche conservatism. Tetraglochin is a genus of shrubs with six species distributed along the Southern and Central Andes, from Peru to southern Argentina and central Chile. Although monophyly of the genus as the identity of its species are well established, spatiotemporal framework for its diversification and the potential role of the ecology and geography in the speciation process remain unknown. In the present study we analyzed diversification times and historical biogeography of the genus, and conducted different climatic niche and geographical range comparisons among its species to determine possible patterns associated with speciation. Results support the Pleistocene diversification, early along the Southern Andes and the Patagonian Steppe and subsequently in the Central Andes. Climatic niche divergence did not prove to be a major factor promoting speciation, but rather the phylogenetic niche conservatism. Our analyses also favored the sympatric model of speciation, although patterns from geographical range evolution are difficult to interpret due to the lability on the ancestral distributions, and therefore micro-allopatric or parapatric divergence associated with the glacial-interglacial cycles and climatic oscillations throughout the Quaternary should not be discarded. Other potential factors associated with diversification of Tetraglochin are also discussed.