"Brain, Behavior and Evolution"

Aristide, Leandro

doi: 10.1159/000552655pmid: 42166386

AbstractIntroduction: Primate brain evolution is characterized by neocortical expansion, yet secondary reductions in brain size have occurred in several lineages. This study reconstructs the evolutionary dynamics of relative neocortex size in anthropoid primates and explores genomic correlates of identified neocortical reductions in New World monkeys to investigate whether such changes reflect direct selection on neural traits or arise from other mechanisms. Methods: Neocortex and medulla volumes were compiled for anthropoid species. Phylogenetic modeling of relative neocortex size was performed using Fabric-regression with medulla volume as covariate. Genomic analyses involved codon-based tests for positive selection (aBSREL) and shifts in selection intensity (RELAX) across 18,177 orthologous protein-coding genes, followed by functional enrichment and characterization of candidate genes. Results: Phylogenetic analyses revealed heterogeneous changes in relative neocortex size across anthropoids, with a statistically significant reduction along the ancestral Callitrichinae + Aotus branch. Genomic scans identified 12 genes under positive selection, two under intensified and none under relaxed selection on this branch, with no enrichment for neurodevelopmental or brain-related pathways. Only a single candidate with potential neurodevelopmental relevance was identified (ZNF512B). Conclusion: The absence of a clear neurodevelopmental genomic signal contrasts with previously reported signatures of positive selection on brain-related genes in encephalized cebids, suggesting that brain expansions and reductions in anthropoids may not share a common genomic basis. This also opens up the possibility that the neocortical reduction detected here emerged as a by-product of selection on other traits (e.g., body size or life-history), rather than as a direct target of selection on neural phenotypes.

Thewissen, J.G.M.; Mars, Katheryn R.; Waugh, David A.; Peacock, John; Stimmelmayr, Raphaela; Citta, John J.

doi: 10.1159/000550974pmid: 41678417

AbstractIntroduction: Ontogenetic brain growth in cetaceans is essential for understanding their development and evolution. This study investigates brain size changes relative to body growth in bowhead (Balaena mysticetus) and beluga (Delphinapterus leucas) whales in the framework of age estimates of pre- and postnatal specimens. Methods: We collected specimens in the field, determined brain size and endocranial volumes, as well as size of endocranial adnexa, either by direct measurement or by CT. We estimated age using baleen length (bowhead), growth layers in teeth (belugas), or fetal stages. We fitted Gompertz growth models to our data. Results: Our findings show that both bowhead and beluga whales reach nearly their full brain size by the end of weaning, unlike dolphins and humans, whose brains continue growing after weaning. Bowhead brains grow faster than those of belugas, and much faster than those of humans, and their rete mirabile occupies a much larger portion of the cranial cavity than in belugas. Encephalization quotients decline with age due to continued body growth after brain maturation. Conclusion: Brain growth in these cetacean species plateaus early, challenging the assumption that cetacean brains grow throughout life. In bowhead, the brain is significantly smaller than the cranial cavity, and this is not the case in beluga. If this observation can be generalized to all mysticetes and odontocetes, it implies that no single equation can capture the proportional volumes of the brain and cranial cavity across the entire cetacean clade.

Pritz, Michael B.

doi: 10.1159/000552475pmid: 42105279

AbstractBackground: Neural circuits form the basis for brain function and behavior. However, solely focusing on adult brains can sometimes overlook prior events that may have shaped this anatomy. These other perspectives can provide further insight into brain circuit organization. Summary: To support this suggestion, specific examples of developmental and genetic events are presented that might not be appreciated if only adult brains were investigated. Examples include the following. One is the origin of nuclei from the same developmental field that divides into major subdivisions. Each of the resulting areas has neurons with different morphology, connections, and molecular signatures. The other is new circuit formation that is produced in three ways. One is the result of peripheral sensory receptor reduction. Another is the consequence of genetic mutation. The third is due to axonal pruning or perinatal injury. Key Message: In certain instances, developmental and genetic features provide additional perspectives to better understand how circuit formation in the brains of adult animals came to be.

Jones, Rachel A.; Higgs, Matthew J.; Isles, Anthony R.

doi: 10.1159/000551100pmid: 41729753

AbstractBackground: Genomic imprinting is an epigenetic phenomenon that, in animals, is found only in viviparous mammals, such as eutherians and marsupials. Differential epigenetic marking of the genomes during gametogenesis leads to parent-of-origin-specific expression of imprinted genes, with some solely expressed from the maternally inherited allele, and others solely expressed from the paternally inherited allele. From an evolutionary perspective, genomic imprinting is fascinating, as it appears to negate the benefits of diploidy and yet correct expression of imprinted genes essential for normal development and function. Summary: Genomic imprinting influences some key mammalian physiologies, including brain and behaviour. Imprinted gene expression is enriched in the “parental hub” neurons of the hypothalamus and the wider defined parental care circuitry. Furthermore, manipulation of a number of these imprinted genes in mice leads to changes in parental care giving. Key Messages: We propose that imprinted genes are likely to influence parental behaviour at several levels. Given their over-representation, it is probable that the recognised “imprinted gene network” operates within the parental hub neurons of hypothalamus. In addition, expression of imprinted genes in the wider brain circuitry, and the pituitary, may modulate different aspects of parental care behaviour. Finally, the known functional consequences of altered imprinted gene expression most likely arise due to changes in the development and/or cellular composition of the parental care circuitry. However, it is clear there remains much to be discovered before we fully understand how and why genomic imprinting shapes nurturing and parental behaviours.

Catania, Kenneth C.; Braun, Christopher B.

doi: 10.1159/000551541pmid: 41838816

AbstractIntroduction: Star-nosed moles are renowned as the fastest foragers among mammals, able to identify and eat small prey in less than a quarter of a second. This ability stems in part from the mole’s extraordinary mechanosensory star which has been the focus of many investigations. However, fast eating also requires a specialized motor system and associated structures. Here, the mole’s unusual incisors are explored as a key adaptation for efficient foraging. Methods: High-speed videos of foraging moles, including microscopic views at 1,000 frames per second, were used to measure prey handling time and tooth movements. Scanning electron microscopy was used to assess tooth structure. Specimens from Cornell Museum of Vertebrates were examined with light microscopy. Data from previous investigations were compared to the present results. Results: A mole with worn front teeth was discovered, and this specimen often failed to secure small prey efficiently, thus doubling the mole’s handling time compared to normal specimens. The manner in which the worn teeth failed suggested the mole’s normal incisors are analogous to a specific type of man-made surgical forceps – so-called Yaşargil tumor forceps. Conclusion: The results reveal an example of serendipitous biomimicry by human surgeons in designing soft tissue forceps, highlight the importance of motor specializations in the star-nosed mole’s fast foraging ability, and suggest some of the specific anatomical specialization that are the result of selection on the key variables (space clearance rate and handling time) in Holling’s pioneering foraging theory equation.

Bruner, Emiliano

doi: 10.1159/000550920pmid: 41662307

AbstractBackground: Humans display larger and more complex parietal lobes, when compared with other primates. The superior parietal lobule is a region still poorly known in terms of comparative and evolutionary neuroanatomy, although at least its medial region, the precuneus, is apparently expanded in our species. Summary: In this article, I review 20 years of personal research on the morphology and evolution of this cortical element. The precuneus is particularly variable among adult humans, mostly in its dorsal and anterior areas. This large individual variability seems already settled at birth. During aging, this cortical region is particularly sensitive to atrophy and neurodegeneration. Its ventral areas are embedded in a complicated topological environment, suggesting spatial, metabolic, and vascular constraints. Key Messages: Human and nonhuman primates share a similar organization of the superior parietal lobule, although with different proportions. Even when compared with extinct hominids, the precuneus in modern humans looks more expanded. These changes are expected to be associated with some cognitive variations, possibly involving visuospatial integration, body cognition, mental imaging, and self-construction.

Heswall, Ariel-Micaiah; Hadden, Peter William; Zhang, Jie; Friesen, Megan; Cain, Kristal E.; Gaskett, Anne

doi: 10.1159/000551766pmid: 41886553

AbstractIntroduction: Many, but not all, bird taxa possess the ability to see ultraviolet (UV) light, but it is currently unclear the extent this ability exists among seabirds. Measuring retinal photoreceptor sensitivity presents many challenges, but the penetration of UV light through the ocular media (ocular transmittance) is a good proxy for UV vision. Methods: Here, we document the ocular transmission of light wavelengths using spectrometry through the eyes of eight Procellariiform and Suliform seabird species found in Aotearoa New Zealand. Results: We report that the eyes of most Procellariiformes, but not the Suliformes, can transmit UV wavelengths. Thus, there is the potential for those Procellariiformes to perceive UV. Discussion: Both phylogeny and ecology could play a role in UV vision in seabirds and understanding the wavelengths that seabirds perceive can be crucial for conservation against visual threats.

Falk, Dean

doi: 10.1159/000552070pmid: 41999614

AbstractBackground: Research on the relationship between the evolution of ontogenetic locomotor milestones and the emergence of advanced cognition in early hominins is reviewed and discussed from an evo-devo perspective that incorporates theoretical underpinnings from the extended evolutionary synthesis. Comparative ontogenetic data from chimpanzee and human infants shed light on likely derivations in hominin locomotor milestones, their effect on the emergence of habitual bipedalism, and the latter’s probable contribution(s) to cognitive evolution. Summary: Human babies’ locomotor milestone of crawling on hands and knees is hypothesized to have been derived during hominin evolution in place of a knuckle-walking developmental stage that likely existed in the apelike predecessors of the earliest hominins. A review of comparative research suggests that evolutionary modifications in crawling, sitting, and pointing in addition to selection for bipedalism, contributed to the progressive evolution of both locomotion and advanced cognition in hominins. Key Messages: Comparisons of the ontogenetic development of locomotor stages in chimpanzee and human infants suggest that locomotor evolution and the emergence of advanced cognition were deeply intertwined during hominin evolution.

Melchionna, Marina; Di Costanzo, Alessia; Morvillo, Linda; Serio, Carmela; Girardi, Giorgia; Castiglione, Silvia; Esposito, Antonella; Raia, Pasquale

doi: 10.1159/000552647pmid: 42166389

AbstractIntroduction: Brain lateralization has deep evolutionary roots in primates, and is often considered to reach its most pronounced expression in humans, particularly in relation to lateralized behaviors. However, little is known about the macroevolutionary dynamics of asymmetric endocranial shape across fossil and extant catarrhines. Here, we apply three-dimensional geometric morphometrics to a comparative sample of extant apes, humans, and fossil hominins to investigate patterns, rates, and directions of brain shape lateralization under an explicit phylogenetic framework. Methods: We analyzed 161 cranial endocasts representing 81 extant and extinct Catarrhine species, using high-resolution geometric morphometrics. We focus on endocast shape lateralization as an evolutionary component of endocranial morphology rather than on individual-level hemispheric differences. Rates of asymmetric shape change are quantified across lineages by using Phylogenetic Ridge Regression (RRphylo) to map evolutionary rates of endocast shape lateralization directly onto the cortical surface. Results: Our results show that hominins exhibit distinctly higher rates of asymmetric endocranial shape evolution compared with nonhuman apes, with particularly pronounced changes observed along the lineage leading to modern humans. These changes are not explained by single-side brain size variation and are spatially concentrated in specific regions of the endocranial surface. Conclusion: The patterns we identified reflect macroevolutionary modifications of endocranial shape and do not constitute direct evidence of hemispheric functional specialization. Nevertheless, the observed evolutionary dynamics are consistent with broader scenarios involving increasing structural reorganization of the brain during hominin evolution. These findings provide a quantitative framework for investigating the evolutionary history of endocranial asymmetry and its potential biological correlates while maintaining a clear distinction between morphological evidence and functional interpretation.

Sansalone, Gabriele; Castiglione, Silvia; Girardi, Giorgia; Dell’Albani, Paolo; Raia, Pasquale

doi: 10.1159/000551768pmid: 41911158

AbstractIntroduction: Similarly sized brains can be made of highly different neuron numbers, which is along the evolution of amniotes multiple shifts in the evolution of the brain size versus brain neurons scaling relationships should have occurred to justify the diversity we observe today. However, if such relationships are conserved within clades, a strong correlation between brain size and brain neurons evolutionary rates should be detected within all clades. Methods: We analysed previously published data of brain and body size and brain neuron numbers of 201 amniotes species spanning from Squamata, Testudines, Aves, and Mammalia. We applied phylogenetic ridge regression (RRphylo) to measure evolutionary rates of the scaling relationship between body and brain size and brain neuron numbers. We employed Bayesian phylogenetic regression and robust phylogenetic regression to understand the evolutionary relationship between each variable. Results: We identified five major shifts in the rates of evolution of neuron numbers. Galloanserae (Aves), Ferungulata (Mammalia), and Primates (Mammalia) showed a positive rate shift, whereas Testudines (Reptilia) and Squamata (Reptilia) showed a negative shift. Furthermore, we detected a marked change in slope and intercept in Primates, Ferungulata, and Galloanserae when compared with Squamata and Testudines. We detected a strong correlation between the evolutionary rates of body and brain size and brain neuron numbers in all clades except for Testudines and a weaker yet significant correlation in Squamata. Discussion: We confirm the presence of a marked shift in the scaling relationships between body and brain size and brain neuron numbers within mammals and birds. Primates display the highest slope, whereas Squamata and Testudines show the lowest. Furthermore, we detected the absence of correlation between the rates of evolution in Testudines and a weaker correlation in Squamata. These results suggest that not all amniotes show similar scaling trends between body and brain size and brain neuron numbers and that coordinated evolution between brain size and neuron numbers is an emergent property only of the most encephalised clades.